GeolCarp_Vol63_No6_491

www.geologicacarpathica.sk

GEOLOGICA CARPATHICA

, DECEMBER 2012, 63, 6, 491—502 doi: 10.2478/v10096-012-0038-y

Introduction

Over the past two decades, a number of studies have empha-
sized the importance of wall structure and cement composi-
tion  as  important  criteria  for  agglutinated  foraminiferal
taxonomy,  leading  to  recognition  of  four  principal  orders:
Textulariida,  Astrorhiziida,  Lituoliida  and  Loftusiida  (e.g.
Desai  &  Banner  1987;  Loeblich  &  Tappan  1987,  1989;
Brönnimann & Whittaker 1990; Hottinger et al. 1990; Banner
et  al.  1991;  Bertram  &  Cowen  1998;  Kaminski  2004a  and
references therein; Bartholdy et al. 2005). Currently, however,
there  is  less  agreement  regarding  the  taxonomic  level  at
which wall microstructure and cement composition ought to
be  used  (e.g.  Mikhalevich  2004),  even  though  modern  re-
searchers do agree that modern microstructural and composi-
tional  studies  on  agglutinating  tests  can  be  used  for  future
taxonomic and paleo-environmental studies.

The genus Colominella Popescu, 1998 was first described

from the Paratethyan Middle Miocene (Badenian) Kostej
(Costei) succession, outcropping in Transylvania (Popescu et
al. 1998; Kaminski 2004b), and is based on a species first de-
scribed by Cushman (1936) from the same locality (type spe-

Selective mineral composition, functional test morphology

and paleoecology of the agglutinated foraminiferal genus

Colominella

Popescu, 1998 in the Mediterranean Pliocene

(Liguria, Italy)

NICOLETTA MANCIN

, ELENA BASSO

, CAMILLA PIRINI

and MICHAEL A. KAMINSKI

4,5

Earth and Environment Sciences, University of Pavia, via Ferrata 1, 27100 Pavia, Italy; nicoletta.mancin@unipv.it

Arvedi Laboratory-CISRiC, University of Pavia, via Ferrata 1, 27100 Pavia, Italy

via Europa 28, 20097 San Donato (MI), Italy

Earth Sciences Department, Research Group of Reservoir Characterization, King Fahd University of Petroleum & Minerals,

P.O. Box 701 KFUPM, 31261 Dhahran, Saudi Arabia

Department of Earth Sciences, University College London, Gower Street, London WC1E 6BT, U.K.

(Manuscript received February 7, 2012; accepted in revised form June 13, 2012)

Abstract: Specimens of Colominella (agglutinated Foraminifera) from a Pliocene Mediterranean succession were analysed
through a scanning electron microscope (SEM) equipped with an energy-dispersive X-ray spectrometer (EDX) to docu-
ment their test microstructure. Colominella develops a complex large test with a mostly biserial chamber arrangement,
but with the internal chamber lumens partitioned by vertical and horizontal plates that form a labyrinthine structure of
alcoves. This internal partition occurs from the first chambers but is completely masked from the outside by the thick
wall. The test-wall microstructure is characterized by canaliculi (parapores) that are externally covered by a pavement
of agglutinated grains. The mineralogical characterization of the agglutinated grains and the secreted cement shows that
the grains are strongly selected as regards to size, arrangement and composition, with the coarse grains placed close to
the outer wall. Moreover, these coarse grains, forming a pavement, are made of monocrystalline quartz, whereas the
inner part of the skeleton is mostly composed of dolomite. The carbonate cement is less abundant and appears as cloudy
light grey areas among the detrital grains. These shell features can be interpreted as functional adaptations to perform
kleptoplastidy and/or to house functional photosymbionts, probably induced by stable environmental conditions as in
warm shallow waters characterized by low nutrient flux.

Key words: Mediterranean Pliocene, photosymbiont, SEM-EDX analysis, grain selectivity, functional morphology,
shell architecture, agglutinated Foraminifera.

cies  Textulariella  paalzowi).  The  same  species  was  subse-
quently reported from the Miocene (Badenian) of the Rauch-
stallbrunngraben,  Vienna  Basin  (Popescu  et  al.  1998).  The
type species is characterized by a very large, elongated, mostly
biserial test, with the inner part subdivided by secondary septa
forming a typical labyrinthine structure and by its caniculate
test wall. Colominella likely evolved from the genus Matanzia
(which  is  also  canaliculate)  during  the  Oligocene  to  Middle
Miocene  (Kaminski  &  Cetean  2011).  Colominella  and  Ma-
tanzia  have  recently  been  placed  in  the  subfamily  Colomi-
nellinae  Popescu,  1998  together  with  other  two  additional
closely-related genera: Colomita Gonzales-Donoso, 1968 and
Cubanina Palmer, 1936 (Kaminski & Cetean 2011).

In spite of this recent systematic review, not much is known

about  the  test  wall  microstructure  of  Colominella  as  regards
the  arrangement  and  chemical-mineralogical  composition  of
the agglutinated grains and the occurrence of other functional
adaptive  morphologies  probably  selected  from  the  environ-
ment in which it lived. This work aims to provide new insights
into Colominella’s test features and to better clarify the rela-
tionship between such a complex test structure and its mode of
life.  Moreover  we  report  for  the  first  time  the  occurrence  of

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Colominella in a Pliocene succession of the Mediterranean area,
thereby extending the known stratigraphical and geographical
range of the genus. Direct comparisons with the type species
from the Badenian of Transylvania were beyond the scope of
this study, therefore, we only tentatively assign the Mediterra-
nean specimens to the species C. paalzowi (Cushman) 1936.

Rationale and methods

The studied section, about 20 m thick, crops out along the

Torsero rivulet in the easternmost portion of the Albenga Ba-
sin (western Liguria) (Fig. 1). This Pliocene Mediterranean
outcrop has been well known since the end of the 19

century

because of its rich mollusc faunas (mainly gastropods) as doc-
umented  by  several  papers  (e.g.  Bernasconi  &  Robba  1984,
1994;  Solsona  1999;  Solsona  &  Martinell  1999;  Andri  et  al.
2005 and references therein; Harzhauser & Kronenberg 2008).
At  its  base,  the  Pliocene  succession  is  composed  of  Lower

Pliocene light grey silty marls belonging to the upper part of
the  “Argille  di  Ortovero”  Formation  (MPL3  foraminiferal
Biozone  of  the  biostratigraphic  scheme  of  Sprovieri  1992),
overlain  by  Middle—Lower  Pliocene  coarse-grained  biogenic
sands, sandstones and conglomerates of the Monte Villa For-
mation (MPL4 Zone) (Violanti 1987). Analyses of both mol-
lusc  and  foraminiferal  associations  clarified  the  depositional
environment  of  the  Argille  di  Ortovero,  which  was  probably
represented  by  the  deeper  portion  of  the  circalittoral  zone,
close  to  the  shelf  edge  (Violanti  1987;  Bernasconi  &  Robba
1994). The Pliocene succession rests transgressively on a Me-
sozoic substratum belonging to the Monte Galero Formation,
a monogenic breccia mostly formed by dolostones and dolo-
mitic limestones (Fig. 1).

For the investigation of foraminiferal assemblages, stan-

dard analytical techniques were used. Six sediment samples,
gathered from the marly portions of the succession (Fig. 1),
were washed through sieves with mesh sizes of 425, 180 and
63 µm, respectively. The residue retained on each sieve was
analysed quantitatively under a stereo-microscope by count-
ing  ca.  300  specimens  from  each  fraction,  as  done  in  the
study by van Hinsbergen et al. (2005). About 50 individuals
(also  including  fragments)  of  Colominella  from  the  > 425
and  425—180 µm  fractions  were  isolated  and  prepared  for
scanning electron microscope (SEM) observations.

In order to assess the internal morphological and composi-

tional features, SEM analyses were performed on the isolated
individuals that had been first embedded in epoxy resin. Resin
mountings were cut in order to obtain a longitudinal section of
the  individual.  The  exposed  test  surfaces  were  mechanically
ground with silicon carbide papers and polished with diamond
pastes at 6, 3, 1 and 0.25 µm, in order to obtain a smooth sur-
face.  Samples  were  then  mounted  on  aluminium  stubs  using
carbon  tapes  and  carbon-coated,  using  a  Cressington  208HR
splutterer. Analyses were performed using a Tescan FE-SEM,
series Mira 3XMU, equipped with an EDAX energy disper-
sive  spectrometer.  Spot  microanalyses  for  standardless  ele-
mental  composition  were  performed  at  15 mm  working
distance, using an accelerating voltage of 20 kV, with counts
of 100 s per analysis. X-ray mapping (stage mapping) for Sili-
con, Magnesium, and Calcium was also done on representative
portions of each individual. EDX elemental maps were acquired
at 20 kV, using a matrix of 256 200 with a DWELL TIME of
200 ms,  16  frames,  1  ADC  and  3  ROIs.  The  EDX  meas-
urements  were  processed  with  the  EDAX  Genesis  software.
For each specimen, SEM-EDX analyses were focussed on:

1) documenting the internal morphological features of the

chambers;

2) measuring the shell thickness and the grain distribution;
3) emphasizing the presence of canaliculi penetrating the

test walls;

4) detecting the chemical composition of the grains and

the cement.

Paleoenvironmental interpretations were based on the char-

acteristics of foraminiferal assemblage composition recorded
in the Rio Torsero succession as proposed by Murray (2006)
and Jorissen et al. (2007). The utilized proxy methods were:

a) proxies of paleobathymetry: the ratio of planktonic to

benthic foraminiferal tests {P = (P/P + B)} as in van Hinsberg

Fig. 1.  Location  and  stratigraphic  log  of  the  Pliocene  Rio  Torsero
section cropping out in the Albenga Basin (western Liguria). A geo-
logical  sketch  map  of  the  Albenga  Basin,  with  the  Mesozoic  sub-
stratum  mostly  formed  by  carbonate  formations,  is  also  reported
(redrawn and simplified by Dallagiovanna & Seno 1986).

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Table 1: Synthesis of the bathymetric distribution and of the ecological and environmental preferences of some benthic foraminifera ob-
served in the modern Mediterranean Sea and used in this work as paleoenvironmental proxies (Jorissen et al. 1992, 1995, 2007; de Stigter et
al. 1998; de Rijk et al. 1999; Schmiedl et al. 2000; Donnici & Serandrei Barbero 2002; Murray 2006). The paleobathymetric subdivision
follows van Morkhoven et al. (1986).

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et al. (2005), completed by the relative abundances of water-
depth benthic indexes;

b) proxies of food availability to the sea floor: Epifaunal/

Infaunal ratio (E/I) and relative abundance of deep and shal-
low infaunal taxa;

c) proxies of substrate: relative abundance of benthic species

indicative of the sediment type (muddy, sandy, mixed), hard
and vegetated surface (epifaunal and phytal taxa) integrated by
lithology and facies variations throughout the succession.

A synthesis of the ecological and environmental prefer-

ences of some benthic foraminifera observed in the Mediter-
ranean Sea and used in this work as paleoenvironmental
proxies (Jorissen et al. 1992, 1995, 2007; de Stigter et al.

1998; de Rijk et al. 1999; Schmiedl et al. 2000; Donnici &
Serandrei  Barbero  2002;  Murray  2006)  are  reported  in  Ta-
ble 1.  The  preservation,  transport  and  reworking  of  benthic
foraminiferal  tests  in  a  mostly  terrigenous  succession  were
also  carefully  evaluated  in  order  to  improve  the  ecological
interpretation.

Benthic foraminiferal taxonomic identifications were

mainly based on the Agip S.p.a.’s Atlas (1982), supplemented
by the works of Cimerman & Langer (1991) and Hottinger et
al.  (1993).  The  benthic  foraminiferal  terminology  used  in
this  work  follows  the  glossary  reported  in  Hottinger  et  al.
(1993).  Foraminiferal  species  abundances  are  reported  in
Table 2a,b (available in the data repository).

Fig. 2. Details of the test architecture of Colominella Popescu, 1998. 1 – Specimen of Colominella from the Rio Torsero section, sample
TOR1; magnification  36; a – apertural face, b – longitudinal view. Note that the internal chamber subdivision into alcoves and the pres-
ence of canaliculi are masked from the outside. Here they are made partly visible by the erosion of the external surface. 2—7 – Details of
the internal partition in alcoves. They are present from the first whorl (2—4) to the last chamber (7); magnification  50. Note that the num-
ber of the alcoves formed by the interposition of vertical plates increases with test growth. 8  –  Details  of  the  alcove  structure,  sample
TOR2; a – alcoves formed by the interposition of horizontal (x) and vertical (y) plates; b – enlargement of “a” showing an alcove with its
typical ovoidal shape. 9 – a – alcoves with trapezoidal shapes, sample TOR1; b – enlargement of “a”: note that also in this case alcoves
are formed by the interposition of two orthogonal plates (x and y, respectively).

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Fig. 3. Detail of the wall microstructure in Colominella. Note that the test wall is crossed by canaliculi with the agglutinated grains selected
in size and distribution. 1 – Detail of the test wall crossed by canaliculi; note that they are externally covered by a pavement, sample
TOR2. 2 – a – Equatorial section of a specimen of Colominella (SEM-BSE image, sample TOR2) showing the typical internal subdivision
into alcoves. Note that canaliculi are limited to the upper portion of alcoves towards the external surface and are missing on the secondary
septa. b – Enlargement of “a”: note that the wall is crossed by canaliculi that are externally covered by a pavement; note also that the larger
grains are arranged close to the external edge forming the pavement. c – Detail of “b” showing the wall microstructure formed by coarse-
grained particles that are embedded by numerous small detrital granules, cemented by calcite that appears as cloudy grey areas among the
grains. 3 – Detail of the wall crossed by canaliculi in a specimen of Colominella sample TOR3. a – Note that canaliculi are mostly straight
and radial internally but become branching in the outer portion of the wall. b – Transverse section of Colominella (SEM-BSE image) showing
the grain arrangement and the occurrence of canaliculi. 4 – a – Equatorial section of a specimen of Colominella (SEM-BSE image, sample
TOR3). b—c – Details of “a” showing the grains selected in size and disposition with the largest ones located near the external margin while
the smallest grains are in the inside. Also in this case canaliculi mostly occur towards the external margin of the alcove.

Results

Shell architecture

The studied Colominella has a quite large, elongate to

fusiform, free test, usually characterized by a circular outline
in equatorial section; the average test dimensions span from
2.5 to 3 mm in length and 1.4 to 1.8 mm in width. The test
shows a mostly biserial chamber arrangement, reported as
triserial in the early stage. The aperture face is formed by the
penultimate and ultimate chamber; the aperture is an internal
marginal slit at the base of the last chamber (Fig. 2.1a—b).

Chambers are partitioned into alcoves, which occur from

the beginning of the shell and continue to the last stage, mak-
ing  a  typical  internal  labyrinthine  structure  (Fig. 2.2—7).  Al-
coves, ovoidal or trapezoidal, are formed by the interposition
of  vertical  (y)  and  horizontal  (x)  plates  (Fig. 2.8—9).  In  the
early stages of the test, alcoves are mostly constituted by the
interposition of vertical plates that form 5 to 6 “chamberlets”,
whereas the interposition of horizontal plates, which increases
the compartmentalization of chambers, occurs later during test
construction  (Fig. 2.2,3,5).  Nevertheless,  the  number  of  al-
coves formed by the interposition of vertical plates increases
throughout  the  test,  reaching  the  number  of  7  to  8  for  each

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chamber in the last growing stages (Fig. 2.5,6). All these fea-
tures are masked from the outside by the rough test surface.

Wall microstructure

The test wall is crossed by canaliculi (“parapores” of Hot-

tinger et al. 1990, 1993) whose presence, just below the surface,
is  revealed  only  in  broken  tests  or  where  the  wall  has  been
partly  abraded  (e.g.  Fig. 2.1b,7;  Fig. 3.1,3a).  Canaliculi  are
straight and radial in the inner portion of the wall but become
branching in the outer part (Fig. 3.1,2b,3a). Moreover, they are
present mostly in the upper portion of alcoves towards the ex-
ternal margin and are missing on the secondary septa (Fig. 2.9b;
Fig. 3.1,2a—b). Canaliculi do not open onto the outer wall sur-
face, because this surface is covered by an external pavement
of  agglutinated  grains  (Fig. 3.2b,3b,4c);  however,  their  open
entrances are clearly visible in the inner surface (Fig. 3.1).

The agglutinated grains are strongly selected in terms of

size  and  distribution.  The  largest  ones  (about  30—50 µm  in
diameter) are arranged close to the external surface forming
a pavement, while the smallest grains are set in the inner part
of  the  wall  (Fig. 3.2b,4b—c).  Moreover,  the  coarse-grained
particles are embedded in an aggregate of very small detrital
granules,  3  to  5 µm  in  size,  cemented  by  a  calcite  cement
that  appears  as  cloudy  light  grey  areas  among  the  detrital
grains  (Fig. 3.2c).  The  grain  selectivity  seems  to  persist
through the whole test.

Chemical-mineralogical characterization

The agglutinated grains are strongly selected not only in

terms of size and distribution, but also on the basis of their
mineralogical composition (Fig. 4). The external particles are
mainly composed of quartz grains (Qz), whereas the internal
ones are made of dolomite (Dol) and a minor amount of cal-
cite (Cc), as indicated by the EDX spectra (Fig. 4a,b,f). In rare
individuals the last chamber is almost totally formed by cal-
cite grains (Fig. 4g,h). All the granules are sub-angular to an-
gular in shape, and the size of quartz and carbonate grains do
not exceed 30 and 50 µm, respectively.

Elemental maps of some major elements were obtained

from a representative portion of the test, in order to observe
their distribution from the outer to inner part of the wall. Sili-
con (Si) and Magnesium (Mg) maps, the discriminating ele-
ments  of  quartz  and  dolomite  respectively,  provide  further
evidence for the placement of different mineral grains in dif-
ferent parts of the test wall. It clearly appears that Si is con-
centrated only in the external portion of the shell, forming a
thin  pavement  that  covers  the  canaliculi  (Fig. 4d,l).  On  the
other  hand,  Mg  is  concentrated  towards  the  inner  part  of  the
wall (Fig. 4e,m). These features are stable during test growth,
occurring from the beginning of the shell to the last chamber.

Characteristics of foraminiferal assemblage composition

Foraminiferal assemblages are abundant, diverse, and well

preserved. They occur together with frequent remains of mol-
luscs, echinoids, bryozoans, ostracods, fish teeth and otoliths.
Toward the top of the studied section in the coarse-grained

Monte  Villa  Conglomerate,  crushed  and  abraded  specimens
increase in number. Foraminiferal associations are very simi-
lar  in  the  first  three  samples  (TOR1  to  TOR3,  Fig. 1)  where
they are strongly dominated by benthic taxa; the plankton per-
centages range from 10 to 15 % (Fig. 5a). Toward the top of
the section (samples TOR4 to TOR6) planktonic foraminifera
slightly increase in abundance reaching values of ca. 25—30 %.
Globigerinoides  (G.  obliquus,  G.  trilobus,  G.  sacculifer,  G.
gomitolus) is the most common planktonic genus with average
percentages  of  ca.  50 %  in  the  planktonic  assemblages,  fol-
lowed  by  Globigerina  (particularly  G.  decoraperta  and  G.
bulloides) and by the species Orbulina universa and Globoro-
talia puncticulata (Fig. 5i, Table 2a).

Benthic assemblages are mostly composed of calcareous

taxa, while agglutinated species usually do not exceed 10—15 %
(Fig. 5h, Table 2b); the latter slightly decrease in abundance
from bottom to top. The most frequent agglutinated species
are:  Lagenammina  sp.,  Textularia  pseudorugosa,  Dorothia
gibbosa  and  Spiroplectammina  wrighti.  Colominella  is
present in very low abundances in samples TOR1 to TOR4,
with  a  maximum  abundance  in  sample  TOR3  (Table 2b).
Calcareous  benthic  foraminifera  are  particularly  abundant
and  well  diversified  throughout  the  entire  succession,  with
over  80  species  recognized  (Table 2b).  In  particular,  phytal
and epifaunal taxa (Fig. 5f—g) strongly dominated the benthic
assemblages  recording  an  Epifaunal/Infaunal  ratio  always
> 2, with peaks of 4 and 6 in sample TOR3, respectively for
the  425—180  and  > 425 µm  fractions  (Fig. 5c).  Shallow  in-
faunal  species  (particularly  Melonis)  are  frequent  (Fig. 5e),
while  deep-infaunal  taxa  (mostly  Bolivina  and  Brizalina
genera) usually do not exceed 12 % throughout the succession
(Fig. 5d). The most abundant benthic specimens belong to the
shallow-water  genera  Ammonia  (A.  beccarii  and  A.  inflata),
Elphidium (E. crispum, E. macellum), large Quinqueloculina
with an ornamentation composed by longitudinal costae (Q.
mediterranensis and Q. vulgaris and less abundant Q. colomi,
Q.  lamarkiana,  Q.  disparilis)  and  to  the  species  Cibicides
lobatulus,  Cibicides  refulgens,  Asterigerinata  planorbis  and
Neoeponides  screibersi  (Fig. 5l—q,  Table 2b).  Other  impor-
tant  components  of  the  benthic  assemblage  are:  Lenticulina
(mostly  L.  calcar),  Heterolepa  bellincionii,  Melonis  affinis
and Melonis soldanii. Deep-water species (indicative of water
depths deeper than 200—400 m; Table 1), such as Cibicidoides
pseudoungerianus,  Gyroidinoides  neosoldanii,  Oridorsalis
umbonatus  and  Trifarina  spp.,  also  occur  but  in  very  low
abundances (e.g.  < 10 %); they slightly increase in abundance
toward the top of the section (Fig. 5b).

Discussion

The genus Colominella developed an agglutinated test that

is  structurally  and  compositionally  very  complex.  This
prompts  the  following  questions:  1)  what  is  the  functional
significance  of  the  complex  structural  and  compositional
features of the Colominella test and 2) what kind of environ-
mental drivers are they associated with?

In the following discussion we address these questions

even if in some cases further investigations will be needed.

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Functional morphologies

Most of the morphological features characterizing the test

of Colominella could be interpreted as a direct expression of

a  strong  relationship  with  the  environment.  These  are:  the
large  free  test;  its  aperture  face,  chambers  internally  parti-
tioned  by  secondary  septa  forming  alcoves,  the  caniculate
test wall; the complex wall microstructure with grains selected

Fig. 4. SEM images of equatorial sections of Colominella and EDX spectra of the agglutinated grains. a—c – BSE images at different mag-
nifications; d—e – elemental maps showing the distribution of Si and Mg respectively in the portion of the Colominella test recorded in
image c; f – EDX spectra of quartz, calcite and dolomite grains; g—i – BSE images of another Colominella individual; h – EDX spec-
trum of a calcite grain; l—m – elemental maps showing the distribution of Si and Mg respectively in the portion of the Colominella test
corresponding to image l.

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Fig. 5.

Characteristics

the

foraminiferal

assemblage

composition

rec

orded

the

Pliocene

Rio

Torsero

succession.

See

the

text

for

further

explanations.

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in terms of size, distribution and composition with an exter-
nal pavement mostly made of quartz.

The large size of Colominella (ca. 3 mm in length and ca.

1.5 mm in width) could represent the first important morpho-
logical  evidence  of  its  interaction  with  the  life  environment.
Larger individuals can be considered as distinctive expression
of  an  environmental  selection  applied  for  longer  times,  as  in
the  case  of  environments  characterized  by  stable  ecological
conditions and by k-strategist relationships. Hottinger (2000)
maintained that the larger an organism, the longer its exposure
to the environment during its life time, the more important are
the  functions  guiding  permanent  morphologies  that  become
necessary for the individual’s survival. Moreover its aperture
face is characterized by a smoothed surface that is not a plane,
but it shows a difference of level between the penultimate and
ultimate  chamber.  We  think  that  Colominella  could  live  at-
tached to a substrate by its apertural end extruding its pseudo-
pods  from  the  gap  between  the  substrate  and  its  penultimate
chamber  (Fig. 2.1a).  According  to  Hottinger  (2006)  as  well,
this feature is indicative of an adaptation to a sessile or poorly
motile life-style, as documented by the occurrence of this kind
of aperture face in some modern textulariids that live attached
to firm substrates in the Red Sea.

Another important piece of morphological evidence is the

internal  chamber  subdivision  into  alcoves  (Fig. 2).  These
spaces within the test are usually utilized to compart the proto-
plasm producing marginal or lateral “quiet zones” in the proto-
plasm itself (Hottinger 2000). It is noteworthy that in numerous
modern  calcareous  foraminifera,  similar  compartments  usu-
ally host algal photo-symbionts (green-house structures), even
though similar structural elements also occur in deep-sea spe-
cies (e.g. Cyclammina) living at too great a depth to host algal
symbionts. In the latter case, alcoves and alveoles have been
interpreted  as  functional  to  better  facilitate  gas  exchange  with
the exterior (Hottinger et al. 1990; Hottinger 2000). However,
in  the  deep-water  species  Cyclammina  apenninica,  the  test
wall  is  never  crossed  by  canaliculi  (Plate 1:  fig. 1b  in  Mancin
2001), on the contrary a caniculate test wall is well developed
in the studied specimens of Colominella (Fig. 3).

Agglutinated foraminiferal canaliculi (parapores) have been

compared  with  the  test-wall  pores  in  hyaline  foraminifera
probably because they serve the same function (Murray 1994).
At  present,  their  function  is  not  so  clear,  but  agglutinated
canaliculi and hyaline pores may be functional for enhancing
gas exchange, for taking and distributing organic matter inside
the test, and/or for accumulating food items in the cytoplasm
(Hottinger  2000).  In  hyaline  foraminifera,  gas  exchange  be-
comes  very  useful  when  they  enter  into  endosymbiosis  with
algal cells; in this case pores are also used to irradiate sym-
bionts  by  sunlight.  For  further  details  on  endosymbiosis  in
foraminifera  see  Lee  et  al.  (2010  and  references  therein).
Canaliculi  could  serve  for  the  internal  diffusion  of  nutrients,
since modern agglutinated foraminifera lack photo-symbionts
and therefore have no requirement for the uptake of carbon di-
oxide or sunlight irradiation (Hottinger et al. 1990).

The studied specimens of Colominella also show a very

complex wall microstructure with the agglutinated grains se-
lected in terms of size and mineralogical composition. Mancin
(2001) documented in Paleogene deep-sea species of Vulvulina

and Karreriella a similar grain arrangement and a marked se-
lectivity in grain composition (e.g. albite in Vulvulina). How-
ever, those deep-sea species did not develop a caniculate test
wall, with canaliculi covered by a distinct pavement made of
quartz  (Plate 3:  fig. 3c  in  Mancin  2001).  In  Colominella  the
test wall is mostly composed of dolomite and a minor amount
of  calcite  and  quartz  (Fig. 4).  The  choice  of  these  minerals
could be simply related to their presence and/or abundance in
the  sea  floor.  The  substratum  on  which  the  Pliocene  succes-
sion deposited is a dolomitic breccia, interbedded with mica-
ceous-quartzitic sandstones (Fig. 1). We believe that the grain
selection cannot be merely a matter of chance or related to the
mineral availability and abundance. Using large quartz grains
to build the external pavement, Colominella could improve its
test robustness with an increase in protective function, an ad-
aptation that would be very useful in  a high  energy environ-
ment  or  in  an  area  with  heavy  predatory  pressure.  Because
quartz is transparent, sunlight would be transmitted across the
pavement and via canaliculi to irradiate the alcoves, above all
in  shallow  water  where  the  light  intensity  is  higher.  Other
studies documented preferential grain selection in modern and
fossil agglutinated foraminifera and a strong relationship with
the environment (e.g. Heron-Allen & Earland 1909; Allen et
al. 1998; Tuckwell et al. 1999; Tyszka & Thies 2001; Armynot
du Chatelet et al. 2008; Thomsen & Rasmussen 2008; Makled
& Langer 2010; Gooday et al. 2010). However,  Colominella
shows  a  grain  selectivity  in  terms  of  arrangement  within  the
test wall as well as the choice of particular minerals to build
the shell, that appears to be stable during its test growth, sup-
porting the idea of genetic control on grain selection.

In the studied Pliocene specimens of Colominella, different

functional  adaptations  co-exist.  They  are  the  expression  of
adaptive responses to persisting environmental selection, as
in the case for hosting photo-symbionts, superimposed on a
genetic basis. At least one modern agglutinated foraminiferal
genus  (Reophax)  is  reported  to  perform  chloroplast  seque-
stration,  also  known  as  kleptoplastidy  (Bernhard  &  Bowser
1999);  that  is  the  ability  of  heterotrophic  organisms  to  pre-
serve  photosynthetically  active  chloroplasts  of  algal  prey
they  eat  and  partially  digest  (Lee  et  al.  1988;  Stoeker  et  al.
2009;  Pillet  et  al.  2010).  We  hypothesize  that  the  Pliocene
Mediterranean  Colominella  could  have  performed  klepto-
plastidy or engaged in some other kind of photosymbiotic re-
lationship.  To  check  this  possibility,  the  paleoecological
parameters  that  probably  affected  the  benthic  foraminiferal
distribution in the studied succession and also influenced the
test morphology of Colominella are discussed below.

Paleoenvironmental limiting factors

The characteristics of the foraminiferal assemblages previ-

ously described (Fig. 5), enable us to gain some insight into
the paleoenvironmental conditions in the Rio Torsero area
during the Early Pliocene. These are:

1) Oligotrophic warm surface waters: these conditions

can be hypothesized considering the strong abundance in the
planktonic assemblages of the warm-water, surface dwelling
Globigerinoides, O. universa, and G. puncticulata (Hemleben
et al. 1989, 1991) throughout the entire succession. These

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GEOLOGICA CARPATHICA, 2012, 63, 6, 491—502; Electronic Table 2 Edition, i

surface  conditions  seem  to  persist  for  the  whole  studied  in-
terval.  Warm  surface  stable  conditions  are  also  consistent
with literature data that report a warm stable climate for the
Early  Pliocene  Mediterranean,  the  so  called  “Pliocene  cli-
mate  optimum”,  till  about  ca.  3.2 Myr  (Thunnel  1979);  a
time-span  characterized  by  the  development  of  faunas  and
floras  with  subtropical  affinities  (e.g.  Monegatti  &  Raffi
2001;  Triantaphyllou  et  al.  2009;  Marques  da  Silva  et  al.
2010; Bertini 2010; Por 2010).

2) Outer shelf environment: the strong abundance of free

and fixed mostly epiphytal taxa such as large Quinqueloculina
with longitudinal costae (Q. mediterranensis and Q. vulgaris),
E. crispum and  E. macellum, A. planorbis and the fixed epi-
faunal  species  C.  lobatulus  and  C.  refulgens  in  association
with other shallow-water indexes (A. beccarii and A. inflata)
is indicative of upper neritic bathymetries as in the vegetated
inner  shelf  environment  (Posidonia  oceanica  seagrass;  Ta-
ble 1).  However,  the  co-occurrence  of  deep-water  species
(Cibicidoides  pseudoungerianus,  Gyroidinoides  neosoldanii,
Lenticulina  calcar,  Oridorsalis  umbonatus  and  Planulina
ariminens),  even  if  with  quite  low  abundances  (Fig. 5b),  is
probably  indicative  of  a  deeper  bathymetry  (lower  neritic  to
uppermost portion of the upper bathyal, ca. 100—300 m), con-
sistent  with  an  outer  continental  shelf  environment.  The
marked abundance of upper neritic taxa is therefore interpreted
as due to their transport from shallower environments. Higher
in the studied section an increase of water depth, probably to-
ward  the  upper  slope  (below  200—300 m),  is  hypothesized.
An  increase  in  both  the  P %  and  the  relative  abundance  of
deep-water  indexes  is  recorded  in  sample  TOR4  (Fig. 5a—b).
Contemporaneously,  a  marked  decrease  or  disappearance  of
some  inner-shelf  indexes,  as  Quinqueloculina  (mostly  Q.
mediterranensis), A. planorbis, C. lobatulus, C. refulgens  and
the  large-size  agglutinated  foraminifera  (Textularia  ponde-
rosa, T. pseudorugosa, Dorothia gibbosa, Reophax spp. and
Colominella), occurred together with an increase of crushed
and  abraded  specimens,  above  all  in  those  with  the  largest
sizes  (Table 2b  –  available  in  the  data  repository).  These
data indicate a rapid deepening within the upper part of the
section  (Monte  Villa  Conglomerate).  Similar  paleoenviron-
mental conditions have been previously proposed by Violanti
(1987) and Bernasconi & Robba (1994 and references therein)
on the basis of both foraminifera and gastropod faunas.

3) Mainly mesotrophic conditions on the sea floor: benthic

assemblages  are  characterized  by  a  very  high  E/I  ratio  and  a
low  percentage  of  deep  infaunal  taxa  (Fig. 5c—d).  Both  these
proxies are commonly used as indicative of low food supplies
to  the  sea  floor,  typical  of  mesotrophic  environments  and
well-oxygenated conditions (e.g. Murray 2006; Jorissen et al.
2007). This interpretation is supported by the low abundance
in  the  studied  samples  of  opportunistic  benthic  species,  such
as buliminids and uvigerinids (Table 2b), that proliferate when
abundant  organic  flux  reaches  the  sea  floor  (Jorissen  et  al.
1992,  1995)  and  also  by  the  absence  of  typical  oligotrophic
larger foraminifera (Amphistegina). These are common in oli-
gotrophic  conditions  of  coeval  shallow-water  successions  in
the  Mediterranean  area  and  still  persist  today  in  the  Aegean
Sea and Levantine Basin (Checconi et al. 2007; Mancin et al.
2009; Triantaphyllou et al. 2009).

4) Substrate with a high terrigenous content, vegetated in

the neighbouring inner-shelf portions

: these features are sup-

ported by the high occurrence of the species Quinqueloculina
mediterranensis,  Elphidium  crispum  and  E.  macellum  that
usually lived in the vegetated zone and, by other shallow-wa-
ter indexes that preferred muddy to sandy substrates, such as
Ammonia and textulariids, and by the high percentage of shal-
low infaunal species, which need soft substrates (Table 1). To-
wards the top of the section, an increase of terrigenous input
could  be  hypothesized  mostly  on  the  basis  of  facies  varia-
tions  and  also  by  the  rapid  turnover  in  foraminiferal  assem-
blages, recording a progressive deepening toward upper slope
environments. The overlying deposits belonging to the Monte
Villa  Conglomerate  are  characterized  by  redeposited  sedi-
ments  mostly  composed  of  coarse-grained  sediments  with
abundant bioclastics intercalated with pelitic levels.

The mode of life of Colominella

The depositional environment reconstructed for the

Pliocene  Rio  Torsero  section  probably  comprised  the  most
external  portion  of  a  warm-water  continental  outer  shelf,
where downslope currents transported shallow-water detritus
(mostly biogenic remains and benthic foraminifera) from the
shallower inner portions. The strong abundance of transported
sediment  with  well  preserved  biogenic  remains  that  are  not
size-selected implies that the coast line was not far away, in-
dicating a narrow continental shelf similar to the present-day
shelf  around  the  Ligurian  coast.  The  innermost  shelf  was
probably vegetated, hosting a large variety of epiphytal taxa,
such  as  in  the  modern  Mediterranean  Posidonia  sea-grass
communities (Murray 2006), but also characterized by a high
terrigenous content. In the studied assemblages, epifaunal taxa
that  lived  attached  or  encrusted  to  firm  substrates  are  quite
rare,  while  free-living  epiphytal  and  shallow  infaunal  taxa
are very abundant.

Nutrient supplies were probably low, typical of an oligo-

mesotrophic environment. This ecological parameter, together
with  the  occurrence  of  substrates  with  high  terrigenous  con-
tent and the lack of widely extended hard surfaces, probably
limited  the  development  of  Amphistegina  assemblages  that
frequently  occurred  in  open  oligotrophic  carbonate  environ-
ments in coeval Mediterranean successions (e.g. Checconi et
al. 2007).

We can conclude that Colominella was an upper neritic spe-

cies, living in the vegetated parts of the inner shelf and that it
could  live  attached  to  macrofaunal  remains.  It  was  a  minor
constituent  of  the  foraminiferal  associations  that  usually  de-
velop  in  environments  with  stable  conditions  (Jorissen  et  al.
1992; Murray 2006; Lee et al. 2010). We also speculate that it
could  perform  kleptoplastidy.  Its  attached  life  habitat  within
the photic zone and association with epiphytal forms in an en-
vironment  with  mostly  oligo-mesotrophic  conditions  to  the
sea floor further implies that Colominella could have housed
functional internal symbionts within its chamber alcoves. By
analogy  with  Early  Jurassic  larger  agglutinated  foraminifera
from Tethyan carbonate platforms which are believed to have
harboured  photosymbionts  (BouDagher-Fadel  2008;  p. 204),
the alcoves of Colominella could have been used for such a pur-

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pose. Its transparent quartz outer pavement would have allowed
sunlight to be transmitted via the canaliculi to irradiate the al-
coves, especially in shallow waters with high light intensity.

Final remarks

Pliocene specimens of Colominella develop an agglutinated

test  that  is  more  complex  in  comparison  to  those  described
by Popescu et al. (1998) from the Middle Miocene of Transyl-
vania.  The  complexity  of  the  agglutinated  test,  in  terms  of
both  internal  shape  and  wall  microstructure  and  composi-
tion, is interpreted as an adaptative response to ecological lim-
iting  factors  that  persisted  for  a  long  time,  as  probably
occurred during the warm Early Pliocene interval in the Medi-
terranean  basin.  In  particular  the  co-occurrence  of  different
functional  morphologies,  such  as:  the  large  size,  the  sessile
style-life, the compartmentalized shell with a caniculate wall
and a transparent test surface, are here interpreted as adapta-
tions to perform kleptoplastidy and/or to harbour symbionts
in order to establish k-strategist relationships that usually de-
velop in stable environments such as in shallow warm waters
with a scarce food supply.

In many lineages of larger agglutinated foraminifera, the de-

velopment  of  complex  inner  structure  is  accompanied  by  a
phylogenetic size increase. The supposed ancestor of Colomi-
nella  was  Matanzia,  which  was  a  deep-water  form  that  be-
came  larger  once  it  evolved  a  canaliculated  wall  structure.
The Middle Miocene type species of Colominella from Tran-
sylvania  probably  inhabited  a  deep  neritic  to  upper  bathyal
environment.  If  indeed  our  Pliocene  Colominella  housed
kleptoplasts, then this behavior represents a modification of
pre-existing structures.

Acknowledgments: We are grateful to Prof. L. Hottinger for
the  helpful  suggestions  on  the  functional  morphologies  of
the  studied  agglutinated  specimens.  Prof.  A.  Gooday
(Southampton)  and  Prof  J.  Tyszka  (Krakow)  reviewed  the
manuscript and are thanked for their helpful comments. This
work was presented at the International Symposium on Fora-
minifera-FORAMS  2010  (September  5—10,  2010  –  Bonn)
and  was  financially  supported  by  the  University  of  Pavia
funds (FAR, or Prof. M. Cobianchi).

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180 mm

)

SAMPLES
TOR 6

8 12 41 0 0 13 0 1

3 78

25.7

TOR 5

16 15 53 0 0 10 1 0

3 98

30.7

TOR 4

6 24 1 1

5 2 0

0 50

16.7

TOR 3

4 32 0 1

3 1 0

0 51

TOR 2

2 16 1 0

3 0 0

0 34

11.3

TOR 1

7 13 23 0 2

2 0 0

1 48

15.9

63 mm

)

63 2 0

6 5 13 0 89

55 4 0

4 4

3 0 70

23.1

31 2 1

1 0 36

28 2 1

2 1

4 0 38

12.6

36 0 0

1 3

0 0 40

13.3

29 2 2

1 2

2 1 39

180 mm

TOR 6

26 22 0

5 1 3 0 1 0 0 0 4

6 13

2 0 2 3

2 0 4 22

7 12 0 3 1 2 1 15 0 1

TOR 5

30 29 0

6 0 0 0 0 1 0 0 5 13

3 10 1 0 0

1 0 1

7 24 18 0 0 0 5 0

8 3 1

TOR 4

6 10 0 12 1 3 1 1 3 0 0 5 26 56

0 0 0 0

8 5 0

0 26

3 2 0 0 1 0

4 0 1

TOR 3

0 24 1 17 2 2 0 0 0 0 1 0 40 33

0 0 0 1 13 2 2

8 13

0 0 0 0 3 0

4 0 0

TOR 2

9 0 13 1 3 0 0 3 0 0 4 23 66

2 0 0 3

6 0 0

0 4 0 0 6 0

6 0 2

TOR 1

2 17 0 10 6 7 0 0 0 2 0 1 23 37

3 0 0 0 11 1 2

1 0 0 0 6 0

7 1 3

0 0 0 2 0 1 0 1

6 0 2 0 0 1 0 3 0 0 0 4 0

0 1 2 0

3 1 1 0 0 0 0 0 0 0 10 0 204

3 7

4 1 0 6 21

225

0 1 0 1 0 0 0 0

3 0 0 1 1 0 0 0 1 0 1 3 0

0 2 1 0

1 1 0 0 0 0 4 0 0 0

2 1 194

1 5

2 0 9 2 19

213

0 0 1 1 0 0 0 0

7 17 0 3 0 0 0 0 1 1 1 1 0 0 10 2 5 2

1 1 2 0 0 0 0 0 0 3

2 0 234

0 5

4 0 3 3 15

249

1 0 0 4 0 0 0 0

9 10 0 0 1 0 1 3 2 0 0 0 1 0 13 0 4 0

4 0 3 0 1 0 5 0 0 0

8 0 237

1 1

3 0 3 4 12

249

1 0 0 1 1 2 1 0 15 12 0 3 2 0 0 0 0 0 0 1 0 0

5 5 1 0

0 2 0 0 0 0 2 1 0 0

9 0 224

1 5 34 0 2 1 43

267

0 2 0 0 0 2 0 0 16 12 0 0 0 0 0 0 2 0 0 1 1 0

5 1 1 0 15 11 3 0 2 0 1 0 3 3 2

3 0 232

7 3

3 1 1 6 21

253

SAMPLES

425 mm

SAMPLES
TOR 6

26 43

0 13

0 123

2 23

0 12

199

1 1

2 0

205

TOR 5

31 38

0 12

1 29

1 10

259

0 1

1 1 11

270

TOR 4

2 56

1 13

1 48

253

0 16 4

1 2 29 282

TOR 3

2 39

0 11

0 72

257

1 4

0 12 4 26 283

TOR 2

4 68

0 13

2 10

2 24

0 37

263

0 14 6

2 6 30 293

TOR 1

2 54

5 13

1 22

0 15

3 70

0 11

255

8 5

3 0 31 286

63 mm

TOR 6

16 1 0 23 0 6

5 0 4 0 0 0 11

4 2

48 0

7 13 0 2 0 16 0 0 5 11 2 0 2 1

3 1 0 4 0 2 0 1 10

1 0 0 0 0 0 5 206

0 0 1 0 1

207

TOR 5

33 1 0 38 0 4

5 0 0 0 2 0

7 9

48 3

6 5 0 0

7 0 0 7

6 5 2 0 0

4 1 1 5 0 0 1 0

7 1 0 0 4 0 5 228

0 0 0 4 4

232

TOR 4

7 0 0

9 0 5 20 0 0 0 5 9

3 0

93 0 11

8 0 1 0

5 2 0 2

9 3 1 0 1

7 5 0 3 5 0 0 0 13 10 1 0 2 0 0 6 254

0 0 1 8 9

263

TOR 3

6 1 0 20 1 4 13 1 0 0 0 0

7 9 105 0

9 0 0 0

3 0 0 0 19 3 0 0 0 24 2 0 1 3 0 1 0

5 10 2 0 0 1 0 3 259

0 0 0 3 3

262

TOR 2

9 0 1 15 0 8 14 1 0 0 2 0

1 2 119 0

9 0 0 0

7 0 0 2 10 4 1 0 0

5 2 0 2 0 0 0 0 13

2 0 0 0 5 0 7 252

1 5 0 2 8

260

TOR 1

2 0 0

8 0 5 22 0 1 2 0 0 12 12 5 118 0

2 10 0 1 0

2 0 1 1 16 0 1 0 0

8 7 1 4 0 0 0 0

0 2 1 0 1 2 7 256

0 0 0 5 5

261

SAMPLES

Table 2:

Numerical database reporting the abundances and distributions of the foraminiferal species detected in the Rio Torsero section.

— Planktonic species;

— Benthic species.

Electronic Edition of Table

—

2a,b

MANCINI et al. PALEOECOLOGY OF

POPESCU, 1998 (LIGURIA, ITALY)

COLOMINELLA

SAMPLES
TOR 6
TOR 5
TOR 4
TOR 3
TOR 2
TOR 1