Journal of Ocean Research, 2019, Vol. 4, No.

1, 6-19
Available online at http://pubs.sciepub.com/jor/4/1/2
Published by Science and Education Publishing
DOI:10.12691/jor-4-1-2

The PETM Extreme Climate Impact on the Benthic

Foraminiferal Traits and Ecological Functioning
in the Tropical Pacific Ocean
Celestine Nwojiji1,3,*, Bryony Caswell2, Fabienne Marret1
1
School of Environmental Sciences, University of Liverpool, L69 7ZT, UK
2
School of Environmental Science, University of Hull, HU6 7RX, UK
3
Department of Geology, Ebonyi State University, Abakaliki, Nigeria
*Corresponding author: [email protected]

Received November 10, 2019; Revised December 12, 2019; Accepted December 25, 2019
Abstract Foraminifera are marine microorganisms which provide essential ecological functions in the oceans.
They are very sensitive to the physio-chemical changes in the marine environment and tend to incorporate the
changes in the environment they lived into their test during calcification. The records of the changes in their test
serves as a black box for the changes in ocean ecology over time. In view of current changes in the global marine
ecosystem as a result of anthropogenic and natural pressures, it is important to understand the reaction of
foraminifera (both at the community level and individual attributes) to the late Palaeocene – early Eocene
hyperthemal event [the Palaeocene-Eocene thermal maximum (PETM)]. The PETM was a global warming event
that occurred 55 million years ago. It resulted in the acidification of the deep sea, shoaling of the lysocline and
Carbon Compensation Depth (CCD), massive extinction of benthic foraminifera as well as diversification and
migration of both marine and terrestrial organisms. This study used Biological Trait Analysis (BTA) to understand
the changes in foraminiferal population and trait composition during the PETM. The results from this study
demonstrated that BTA techniques could be used to detect ecological disturbance based on non-metric
multi-dimensional scaling (nmMDS) ordination. The nmMDS ordination of all the studied sites showed wider
separation during environmental disturbance [period of negative Carbon Isotopic Excursion (CIE)] compared to
other intervals. Thirteen (13) foraminiferal traits and over 60 trait categories were perceived to be crucial for the
foraminiferal ecological functioning in the marine environment. However, BTA recognised test composition,
chamber arrangement/ shape, ornamentation, primary aperture position, perforations and living/feeding habit as the
most important foraminiferal trait in the benthic ecosystem. Traits such infauna and sessile life habits; cylindrical
elongate and bi-triserial test forms; complex terminal apertures and omnivorous feeding modes were the most
resilient traits during the hyperthermal.
Keywords: PETM, benthic foraminifera, palaeooceanography, palaeocology, extreme climate, biological traits
Cite This Article: Celestine Nwojiji, Bryony Caswell, and Fabienne Marret, “The PETM Extreme Climate
Impact on the Benthic Foraminiferal Traits and Ecological Functioning in the Tropical Pacific Ocean.” Journal of
Ocean Research, vol. 4, no. 1 (2019): 6-19. doi: 10.12691/jor-4-1-2.

the next 100 – 500 years based on the assessments of

fossil fuel reserves and other resources is 5000 pentagrams
1. Introduction of carbon [6,7,8]. A Similar scenario of CO2 in the Earth
system was recorded during the Palaeocene – Eocene
The rate at which species are disappearing in the thermal maximum (PETM) 55.6 million years ago. The
biosphere due to the current climate change has made PETM is one of the most significant climatic events in the
the scientific community propose that if mitigating last 90 million years of Earth history [9]. The hyperthemal
circumstances are not put in place, the Earth will be was caused by the release of enormous 13C depleted
approaching the sixth mass extinction before the end of carbon into the Earth system carbon pool. The source of
the century [1]. The primary driver of current climate this carbon included the greenhouse gases emitted from
change is the emission of carbon dioxide (CO2). The dissociation of methane clathrates from the sea floor
understanding of the impact of extreme climate on marine [10,11], large igneous provinces e.g. during the opening of
biodiversity resulting from increased greenhouse gas input the North Atlantic basin [12], and thermogenic emissions
into the oceans is critical to the understanding of how the of carbon dioxide from decaying organic matter [13]. The
Earth systems will function in the near future [2,3,4,5]. dissolution of these gases in the ocean and the increases in
The estimated CO2 concentration of the earth system for their atmospheric concentration raised the temperature of
 Journal of Ocean Research 7

the global surface oceans to 9°C and 5°C in the bottom By definition, trait is the total constitution, physical
water in a relatively short period of geological time ~10, appearance and behaviour of an organism while biological
000 years [14,15]. In addition, the rise in temperature trait analysis is a multivariate statistical approach used to
resulted in other major environmental and biological describe species distribution, their biological characteristics
changes including acidification of the deep ocean, global and how it is related to the running of their ecosystem [31].
expansion of oxygen minimum zones and local photic This new approach was used to examine the benthic
zone euxinia, sea-level rise, significant shoaling of the foraminiferal data generated from two different oceans in
global ocean carbonate compensation depth (CCD), an order to understand the biotic and functional turnover
accelerated hydrological cycle and most importantly, based on the trait composition of foraminifera. The
species biogeographic migrations and the disappearance of ecological functioning of foraminifera have been inferred
30-50% of intermediate – deep-sea benthic foraminifera based on their traits changes during the hyperthermal.
[16-21]. The key questions answered by this study include;
The principal expression of the PETM in the geological 1. Are there evidence of trait changes in foraminifera
record is the benthic foraminiferal extinction (BEE), a during the PETM
large and rapid negative carbon isotopic excursion (CIE) 2. Does any pattern exist in the trait composition of
from both the marine and terrestrial environments [22]. benthic foraminifera during the PETM in the tropical
There has been a series of debates over which of the Pacific?
climatic feedbacks caused the extinction of benthic 3. Did changes in the traits of benthic foraminifera
foraminifera: whether it was ocean acidification, rises in coincide with the changes in taxonomic composition?
water temperature, changes to nutrient supply or 4. How did the faunal turnover of benthic foraminifera
deoxygenation of the bottom water. This study will and their traits affect the ecological functioning of the
contribute to this debate by investigating if trait changes in benthic system during the PETM?
foraminifera during the event played a role in the benthic 5. Which traits were resilient or susceptible to changes
foraminiferal extinction. during the PETM?
Foraminifera are important in the functioning of marine
ecosystems and ocean biogeochemical cycles such as
organic carbon export as 60% of deep sea sediment compose 2. Materials and Methods
of their test. They link the primary production from
phytoplankton to the higher trophic levels – shrimps, 2.1. Data Sources and Site Descriptions
fishes, mammals and seabirds hence are critical components
of the trophodynamics of benthopelagic ecosystems [23]. The data for this study was derived from the previously
Most of the micropalaeontological techniques used in published foraminiferal census of ODP leg 198 sites
understanding the impact of extreme climate on biotic 1209B and 1212B by [32]. The foraminiferal census data
turnover in deep-time were based on taxonomic as used to generate a new trait composition data of
assemblage, specific species analysis and geochemical individual species (see the supplementary data). The cores
data [18,19,24-29]. These have provided significant from ODP 198 were located in the southern high area of
insight to the events nevertheless, faunal assemblage data the Shatsky Rise (Figure 1) along a prograding water
are prone to error due to poor preservation that may result depth transect of 500m [33]. Thirty (30) sediment samples
from the taphonomic processes [30]. Hence, this study each were analysed from a 30cm length of core across the
explores the use of trait-based approach [Biological Trait PETM interval at sites 1209B and 1212B. The sediments
Analysis (BTA) technique] in understanding how traits consist largely of nannofossil ooze with a distinct dark
and ecological functioning of foraminifera changed across brown clay-rich interval that marks the core of the PETM
the Palaeocene – Eocene Thermal Maximum (PETM). and the P/E boundary [32].

Figure 1. Late Eocene palaeogeographic map showing the studied sites. 1-ODP Leg 198 Shatsky rise (Sites1209B &1212B)
8 Journal of Ocean Research

2.2. Trait Classifications and Analytical their spines and gaining sufficient nutrient from them. In
Procedures general ornamentation in foraminifera play a huge role in
feeding, adaptation to extreme environmental condition,
The foraminifera species in the census data [25,32] movement as well as prey -predation relationship. A study
were classified into thirteen different biological categories by [38] demonstrated that foraminifera (Haynesina
(Table 1). The traits selected were those considered to germanica) use body ornamentation to sort food particles
reference core ecosystem functions or processes in the into different shapes and sizes thereby removing harmful
ocean that may be provided by foraminifera. Important substances as well as disaggregating larger particles into
traits that can provide an index for some of these smaller pieces before ingestion [38]. It is a great adaption
ecosystem functions include basic aspects of test for escaping from predators. The form of apertures, the
composition, morphology such as the test shape, chamber presence of accessory structures and their primary position
arrangement, chamber shape, wall structure and living vary with change in environmental condition. For instance,
habit. at ambient water chemistry, Haynesina germanica had
Foraminiferal test composition varies from agglutinated a well-developed apertural face, teeth, tubercle and
materials to secreted calcite and could indicate changes in umbilical area but these features were difficult to identify
the ambient environmental chemistry and composition in species found in extreme CO2 and pH levels [38].
[34]. Foraminiferal test composition functions as a The perforation of foraminiferal test is a critical
protective tool and is known to reduce biological, physical functional feature of the organism; they could be coarse
and chemical stress in their environment [35]. The test exceeding 10µm or fine ranging from 1µm to a few tenths
shape could indicate ecological adaptation and preference of micro-millimetres. Pores in foraminifera are used for
by foraminifera. Spiral tests have been associated gas exchange, osmoregulation, intake and release of
with epifaunal habitat [36], they are characterised by nutrient and ecosymbiosis. Large pores are possessed by
plano-convex – bi-convex trochospirally coiled test with species in a well-oxygenated environment while species
large pores (e.g. Gavelinella beccarriformis). The shallow found in the low oxygen environment have smaller pores
infaunal taxa are usually elongate, uniserial to triserial [39]. They allow the organism to attach to hard substrate
chambered or planispirally coiled (e.g. Dentallinid or by secreting some organic adhesives through them.
Buliminid) while the deep infauna are ovate (globose) to Characteristics of foraminiferal behaviour such as their
triserial which are common in imperforate taxa such as life habit (whether they live infaunal or epifaunal), feeding
Oolina globosa; Tapanina selmensis. The arrangement of habit and mobility may indicate their level of tolerant
the test chambers and their shape chamber could also to prevailing water chemistry, nutrient and oxygen
indicate ecological stress, for instance, change from concentration and other hydrodynamic conditions.
sinistral to dextral or evolute to involute coiling in These traits (mentioned above) were each classified
trochospiral test has been related to change in water into subcategories referred as modalities (Table 1), for
temperature and bathymetry [37]. Elements of test instance, test shape is classified into spiral, elongate,
microstructure such as the test macro-ornamentation globose, tubular, subquadrate, and others. This
(e.g. spines) could also reflect the mode of living and categorisation is not exhaustive but highlighted the
adaptation to surrounding water condition. Spinose modalities that are; common in the recovered species,
species of living foraminifera are known to be symbiotic, quantifiable or those available in the accessed literature
harbouring photosynthetic alga like dinoflagellates within and databases.

Table 1. Example of traits and associated modalities used in biological traits classification of foraminiferal communities

Traits Modalities
A. Test Shape A1. Spiral A2. Elongate A3. Globose A4. Tubular A5. Others
B2. Hyaline B3. Hyaline B4. Secreted:
B. Test Composition B1. Agglutinated B5. Others
calcite aragonite Porcellanous
C. Chamber arrangement C1. Unilocular C2. Uniserial C3. Bi/Tri-serial C4. Planispiral C5. Trochospiral C6.Other
D3. Triangular or
D. Chamber shape D1. Spherical/Oval D2. Tubular D4. Semi-circular D5. Others
trapezoidal
E2. Raised
E. Test macro-ornamentation E1. Depressed sutures E3.Ponticuli E4. Keeled E5. Others
sutures
F. Test micro-ornamentation F1. No ornament F2. Spinose F3. Striate F4. Costae F5. Others
G. Aperture form G 1. Oval/reniform G2. Arcuate G3. Radiate G4. Slit-like G5. Others
H. Aperture accessory structures H1. Lips H2. Teeth H3. Neck H4. None
I2. Basal
I. primary aperture position I1. Terminal I3. Umbilical I4 Extra-umbilical I5. Others
interiomarginal
J2. Fine J3. Coarse
J. Test perforation J1. Microperforation J4. no perforation
perforation perforation
K2. Benthic K3. Benthic
K. Life habit K1. Benthic epifaunal K4. Others
shallow-infaunal deep- infaunal
L. Feeding habit L1. Deposit feeder L2. Herbivore L3. Omnivore L5.Others
M. Mobility M1. Stationary M2. Mobile M3. Clinging M4. Others
 Journal of Ocean Research 9

Table 2. Example list of eight foraminiferal taxa from site 1209B with the fuzzy trait coding for 2 (test shape and chamber arrangement) out of
the 13 traits used for this study
A1. A2. A3. A4. C1. C2. C3. C4. C5.
Modality
Spiral Elongate Globose Tubular Unilocular Uniserial Bi/Tri-serial Planispiral Trochospiral
Anomalinoides
1 0 0 0 0 0 0 0 1
trinitatensis
Bolivina inconspicua 0 1 0 0 0 0 1 0 0
Quadrimorphina
1 0 0 0 0 0 0 1 0
profunda
Oridorsalis
1 0 0 0 0 0 0 0 1
umbonatus
Nuttallides truempyi 1 0 0 0 0 0 0 0 1
Gyroidinoides spp. 1 0 0 0 0 0 0 0 0.5
Laevidentalina spp. 0 0 0 1 0 1 0 0 0
Aragonia spp. 0 1 0 0 0 0 1 0 0

A fuzzy coding [40] technique was used to express the dominant species on the overall result. The similarities of
affinity of different species to the different trait modalities both species and biological traits between samples were
using a scale of 0.0–1.0. The absence of an affinity for a calculated using Bray-Curtis index to create resemblance
particular trait is denoted with 0 whereas 1 is used to code matrices. Non-metric multidimensional scaling (nmMDS)
a species that exhibited a high affinity to a trait (Table 2). was used to visualise the similarities/differences in species
This coding technique allows species that exhibited more and trait composition between the different sections of
than one modality to be categorised according to their CIE. Species/taxa composition and biological trait
affinity (e.g. Table 2), however all the categories shall composition were compared using Analysis of Similarity
sum to one [5,41,42]. (ANOSIM), and subsequently, the similarity percentages
The information on the biological traits were sourced (SIMPER) routine was used to identify which taxa or
from the biological database such as WORMS – World traits contributed the most to differences identified from
Register of Marine Species: http://www.marinespecies.org, the ANOSIM across the PETM.
The Palaeobiology database http://palaeodb.org;
Fossilworks http://fossilworks.org/, Pangaea
https://www.pangaea.de/and Atlas of Paleogene 3. Results
Cosmopolitan Deep-Water Agglutinated Foraminifera
http://nhm2.uio.no/norges/full/atlas/pecol_text.htmp 3.1. Changes in Taxonomic Composition at
published literature (e.g. [43,44]). Review of these data ODP Site 1209B
resources as well as morphometric measurements of
specimens, and personal communications with experts on The majority of the benthic foraminiferal assemblages
a range of taxa informed the coding of traits selected for recovered from Site 1209B are dominated by calcareous
this analysis. taxa and very few agglutinated forms such as Bathysiphon
In some species, traits like mobility or feeding habit spp., Spiroplectammina spp., and Tritaxia spp. [32].
could not be directly established because they are already Epifauna taxa accounted for about 14% of the total faunal
extinct with no record of the life history in the literature. abundance and are characterised by Anomalinoides,
In such cases, the indeterminate traits were extrapolated Cibicidoides, Oridosalis, Gavelinella and Gyroidinoides
from the closest relative (at the genera or family level) or taxa. Infaunal morphogroup constituted over 80% of the
from the functional morphology of a known taxa. For total abundance and was dominated by the Buliminds with
instance, if the chamber form of a species was rounded 50% of the total abundance [32]. The pre-CIE interval of
trochospiral, Nagy’s (1995) functional morphology principles the PETM at site1209B was characterised by a
were applied to indicate that the species was probably a predominance of Bolivina inconspicua, Bulimina kugleri,
superficial epifauna and may have been a deposit feeder Paralabamina spp., Gavelinella spp., Gyroidinoides spp.,
(see http://nhm2.uio.no/norges/full/atlas/pecol_text.htm), Lenticulina spp., Siphogenerinoides brevispinosa,
though this was on a very rare cases. Fursenkoina sp. and the Stilostomellids. Most of these
The frequency of each trait modality in the dataset was taxa disappeared at the peak of the CIE [32]. The CIE
determined by multiplying the trait modality scores by the interval was characterised by the acme of Bolivina gracilis,
relative abundance of each species exhibiting those Anomalinoides trinitatensis, Buliminella cf. beaumonti,
modalities in each sample. This was achieved by matrix Globocassidulina subglobosa, Quadrimorphina halli, Q.
multiplication [42]. pacifica, Q. profunda, Quadrimorphina sp. 1, Tappanina
Statistical analyses of both taxonomic abundance and selmensis and Bulimina bradburyi. The recovery section
trait composition were performed with PRIMER v. 6 recorded the highest relative abundance of foraminifera
(PRIMER-e, Plymouth, UK). Prior to the statistical and was dominated by Bulimina spp., Nuttallides
analysis, data were subdivided into three to reflect the truempyi, Bulimina bradburyi and Pleurostomellid taxa.
stages in CIE (Pre-CIE, CIE and Recovery) event. The The detailed faunal composition has been discussed in [32]
pre-analysis treatment of the samples required and the focus here is using the BTA to understand the
standardisation of the species data which were changes in taxonomic composition in relation to changes
transformed with Log (x+1) to reduce the influence of in trait composition.
10 Journal of Ocean Research

Figure 2. Non-Metric Multidimensional Scaling ordination of foraminiferal taxonomic composition (transformed with log x+1) of Bray-Curtis
similarity. A- Samples from ODP Site 1209B Shatsky Rise, Pacific Ocean. B- Samples from ODP Site 1212B Shatsky Rise, Pacific Ocean. Colours
indicates samples from the three intervals the PETM (Pre-CIE, CIE and Recovery)

Table 3. Mean abundance of species contributing to the most dissimilarity between the three PETM intervals at Site 1209B (50 % cut off).
Mean abundance
Species % Contribution
Pre-CIE CIE REC
Quadrimorphina profunda 1.45 27.66 17.96 17.41
Bulimina kugleri 20.27 1.79 0.12 12.47
Bolivina gracilis 0.33 11.87 1.83 8.13
Bolivina inconspicua 12.3 2.08 0.07 7.63
Oridosallis spp. 9.29 1.92 4.98 5.31
Buliminids 12.5 14.92 30.79 13.63
Pleurostomellid spp. 1.14 3.1 11.41 7.52
Nuttallides sp. 5.99 4.59 13.39 7.61
Nuttallides truempyi 4.27 4.59 13.39 5.64

Non-metric multi-dimensional scaling (nmMDS) ordination during the CIE (Table 3). During the recovery period, half
of the recovered benthic foraminiferal assemblages as many Quadrimorphia profunda and ten-fold less
(Figure 2) showed three clear taxonomic groupings during Bolivina gracilis occurred compared with the CIE period
the pre-CIE, CIE and the recovery. ANOSIM values (Table 3). Whereas Buliminids, Nuttalides truempyi and
confirmed that the three groups significantly differed Pleurostomellid spp increased. The recovery assemblage
(global R= 0.693; p<0.01) and pairwise ANOSIM with also differed from the pre-CIE in having less B. kugleri
p<0.01 also showed that all the three groups significantly and B. inconspicua, Buliminids, Quadrimorphina
differed from each other. However, the taxa from 196.455 profunda, Pleurostomellid spp. and Nuttallides truempyi
mbsf (classified as CIE based on the carbon isotope) than pre-CIE (Table 3).
ordinated closely with the pre-CIE. Taxa in sample
196.445 mbsf ordinated at the centre of the three 3.2. Changes in Foraminiferal Trait
groupings while taxa in 196.435 mbsf was an outlier. The Composition at ODP Site 1209B
reason for the outlier was that foraminiferal specimens in
sample 196.435 mbsf was lowest in number when Similar to the ordination for taxonomic composition,
compared to other samples and not up to 100 specimen. the trait composition (Figure 3) differed between the three
Also, the benthic foraminiferal extinction event (BEE) that intervals of the PETM as shown by the global R = 0.581
marks the onset of the CIE occurred at this sample depth. and p<0.01. Pairwise ANOSIM indicated that the
The three samples that did not ordinate with their group composition present during the recovery period
could be evidence of the severe environmental changes significantly differed (p<0.01) from both those preceding
that occurred at the beginning of the CIE [32]. it. The trait assemblages present during the pre-CIE
Similarity percentage (SIMPER) between the pre-CIE significantly differed from those present during the CIE
and the CIE intervals (at 50% cut off) showed that only although at lower significance (p>0.01). Overall trait
five taxa (Table 3) contributed to the most dissimilarities composition during the recovery was more similar to the
in site 1209B. The taxa contributing to the dissimilarity CIE than at the pre-CIE (Figure 3) as was the case for
were Quadrimorphia profunda and Bolivinia gracilis taxonomic composition. The trait composition of samples
which was 20-fold more during the CIE than at the from depth 196.455, 196.435 and 196.445 mbsf ordinated
pre-CIE. Bulimia kugleri was also 20-fold less during the away from the CIE group they belonged to. These are the
CIE than at the pre-CIE while Bolivinia inconspicua and first few samples at the beginning of the CIE and may be
Oridosallis spp significantly decreased in abundance an evidence of biotic disturbance associated with the event.
 Journal of Ocean Research 11

Figure 3. Non-metric Multidimensional Scaling ordination of foraminiferal traits composition (transformed with log x+1 and total resemblance) of
Bray-Curtis similarity. A- Samples from ODP Site 1209B Shatsky Rise, Pacific Ocean. B- Samples from ODP Site 1212B Shatsky Rise, Pacific Ocean

Figure 4. Similarity percentage (SIMPER) with traits that contributed to the differences in benthic foraminiferal trait composition across the PETM
events in the studied sites (Data cut off 50%).. Grey bars = Pre-CIE; sky blue bars = CIE core; deep blue bars= Recovery

SIMPER results also showed that 19 traits (at 50% cut elongate tests; hyaline calcite and hyaline aragonite tests;
off) contributed to the dissimilarity between intervals bi/triserial and planispiral chamber; spherically shaped
(Figure 4) all of which were more abundant during chambers, depressed sutures, costate ornamentation, fine
the recovery than pre-CIE, these included spiral and perforations and bifid teeth. Foraminifera with apertures at
12 Journal of Ocean Research

the terminal and umbilical positions that lived a sessile global R =0.649, and that each group significantly differ
lifestyle and shallow – deep infauna also contributed from the other at p<0.01. The pairwise ANOSIM tests for
significantly to the dissimilarities. The mean abundance of the three intervals showed that the taxonomic composition
taxa with spiral coiling, hyaline aragonite test, planispiral of the assemblage significantly differs as follows:
chamber arrangement, no apertural accessories, aperture at recovery and CIE R= 0.317, p<0.02; recovery and pre-CIE
the umbilical position and lived shallow infauna were R= 1, p< 0.02; CIE and pre-CIE R= 0.683; p<0.1. During
higher during the CIE than at any other interval of the the CIE there was a wider separation between samples
PETM. After the CIE, the benthic communities seem to (SIMPER, 53% similarity) compared with the pre-CIE
become more successful than before the CIE, as shown by (SIMPER, 74% similarity) or the recovery (SIMPER, 76%
the high abundance of most of the trait modalities at the similarity). This may be due to the high level of ecological
recovery (Figure 4). The higher abundance of the traits at stress recorded during the PETM warming
the recovery interval may be due to the bloom of The nmMDS plot also showed six subgroupings: one
foraminifera after the hyperthermal. each for the pre-CIE and the recovery, and four subgroups
for the CIE. These subgroupings of samples during the
3.3. Changes in Taxonomic Composition CIE could imply that there may have been a number of
distinct environmental changes during the PETM. Overall
at ODP Site 1212B ordination shows a horseshoe (Figure 2) structure
The recovered taxa from site 1212B were dominated proceeding from the pre-CIE, through several substages of
by cosmopolitan foraminifera, mostly of calcareous test the CIE, and then the recovery. The recovery samples
[32]. The foraminiferal census data [32] showed that showed a clear separation from the pre-CIE and CIE
Siphogenerinoides brevispinosa, Stilostomellids, Bulimina groups.
kugleri and Bolivina inconspicua were present at the Depth 79.745 mbsf which was classified within the
pre-CIE section but disappeared during the PETM. recovery interval (using the carbon isotope curve) but
However, Quadrimorphina profunda, Tappanina selmensis, ordinated with one of the CIE groups, meaning that it was
Bolivina gracilis, Anomalinoides trinitatensis and similar in composition to this subgroup of the CIE than
Laevidentalina spp. recorded their highest abundance the recovery. The transitional nature of the sample from
during the CIE while Eponides elevata was a local 79.745 mbsf suggests that even although δ13C may have
excursion taxon that appeared towards the end of CIE. started to recover to the background levels, the benthic
The ordination of samples from site 1212B in the communities were yet to recover from the ecological
nmMDS (Figure 2) showed three distinct groupings with stress caused by the hyperthermal.

Figure 5. Composite trait variations across the three studied sites. The figures show some trait similarities in trait composition across the two oceans.
The colour used in a particular modality is uniform across all the sites. The trait abundance below each plot represents the absolute count of traits after
standardization. Site location and core depths are plotted at the left-hand corner of the figure and the PETM events at the right
 Journal of Ocean Research 13

Table 4. Mean abundance of species contributing to the most dissimilarity between the three PETM intervals at Site 1212B (50 % cut off).
Mean Abundance
Species %Contribution
Pre-CIE CIE Recovery
Quadrimorphina profunda 0.32 26.89 11.39 18.29
Nuttallides truempyi 4.34 5.68 14.61 8.81
Bolivina gracilis 4.2 9.76 1.32 8.5
Laevidentalina spp. 6.18 5.18 11.4 7.09
Bulimina bradburyi 0.35 1.5 8.33 6.73
Siphogenerinoides brevispinosa 30.44 6.39 0 6.2
Bulimina kugleri 8.67 3.18 0.07 6.72
Bulimina thanetensis 10.75 2.02 2.23 7.2

Results of the SIMPER showed that only five taxa 79.825mbsf lay separately from the rest (Figure 3). The
accounted for 56% of the dissimilarity between the CIE clustering of the CIE samples into three groups could be
and recovery interval (Table 4). During the CIE there were evidence of environmental perturbation during the
relatively higher abundances of Q. profunda and Bolivina hyperthermal, and the outlier (sample 79.825mbsf) marks
gracilis, whereas, during the recovery Buliminids, the BEE interval.
Pleurostomellids and N. truempyi were two to four times Trait distribution deduced from raw data before
more abundant (Table 4). statistical analysis (Figure 5) indicated that species with
The four taxa that accounted for (50% cut off) of the spiral test shape, and planispirally test blossomed during
dissimilarity between the pre-CIE and the CIE were the main period of the CIE when global temperature was
Bulimina thanetensis, Siphogenerinoides brevispinosa, highest. A coeval increase in species with tubular shape,
Quadrimorpha profunda and Bolivinia gracilis. Bulimina arcuate apertures, fine perforations, shallow infaunal life
thanetensis and Siphogenerinoides brevispinosa were habits as well as sessile lifestyle was also recorded at the
more abundant during the pre-CIE than in other sections CIE interval. While species with elongate tests,
while Quadrimorpha profunda and Bolivinia gracilis were agglutinated forms, uniserial chamber arrangement,
more abundant during the CIE (Table 4). The differences terminal apertures, and coarse-perforation increased in
in abundance of Siphogenerinoides brevispinosa and relative abundance at the pre-CIE, but their abundance
Quadrimorpha profunda together accounted for about 40% plummeted drastically with further warming close to the
of the dissimilarity between the two intervals. CIE section.
The taxonomic composition of the recovery interval The similarity percentage analysis (SIMPER) showed
differed from the pre-CIE by containing more Buliminids, that 24 trait modalities accounted for (50% cut off) the
Pleurostomellids, Q. profunda and N. truempyii. In dissimilarity between the three PETM subdivisions
contrast, pre-CIE had higher abundances of B. kugleri and (Figure 4). Six traits predominated at the pre-CIE, these
B. inconspicua (Table 4) than the recovery. include elongate tests, uniserial chamber arrangements,
terminal apertures with neck, agglutinated tests, fine
3.4. Changes in Foraminiferal Trait perforation and semi-circular chamber shape. Taxa with
spiral tests, fine perforation, planispiral coiling, umbilical
Composition at ODP Site 1212B
apertures, no ornament, arcuate shaped apertures and
The nmMDS ordination of trait composition showed grazers that live in the shallow infauna niche were more
that the pre-CIE, CIE and recovery intervals were clearly abundant during the CIE (Figure 4). The recovery interval
separate from each other (Figure 3) and ANOSIM showed recorded the highest abundance of trochospiral test shape,
that they significantly differed at global R = 0.542 and triangular/trapezoid chambers, slit-like apertures, and
p<0.01. The section analysed during the recovery was basal interiomarginal apertural position, non-perforated
short and did not show a significant change in the test and deposit feeders. During the period of recovery,
foraminiferal composition. almost all the species with coarse-perforations in their test
Pairwise ANOSIM showed that the trait composition of and semi-circular chambers that was present during the
the assemblage present during the pre-CIE and the CIE pre-CIE had disappeared from the trait composition
differed significantly at p<0.01. The recovery and CIE (Figure 4).
also differed but at lower significance (p<0.04). During Other trait modalities that were predominant at the pre-
the CIE, samples were highly variable as shown by the CIE but decreased in abundance during the recovery
lowest percentage (79%) in SIMPER group similarity, the include elongate shape, uniserial test arrangement,
pre-CIE samples were 88% similar, and the recovery terminal apertures, and agglutinated tests (Figure 4).
sample similarity was 91%. Nevertheless, there was an increase in taxa with deposit
The nmMDS for trait composition was very similar to feeding habit, umbilical apertures and spiral test during
that of the taxonomic composition. The main CIE the recovery.
ordinates in three subgroups (Figure 3) with samples from The most affected traits at Site 1212B during the peak
depth 79.865 – 79.895 mbsf ordinating within one of the CIE were trochospirally coiled, semi-circular
subgroup, samples from depth 79.755 – 79.815mbsf chamber shape, benthic epifauna and suspension feeding
clustered fairly together, and depth 79.835mbsf -79.845 taxa as shown in Figure 4. However, species with sessile
mbsf formed the third subgroup between the other two lifestyle, deposit-feeding habit and depressed sutures did
CIE subgroups. Samples from depth 79.785mbsf and not show any significant changes across the studied
14 Journal of Ocean Research

interval, and these could be the traits that sustained could be as a result of preliminary increase in the surface
ecological functioning during the hyperthermal (Figure 4 productivity encouraging more phytodetrital rain to the
& Figure 5). sea floor but when the further rise in temperature resulted
to enhanced metabolic efficiency of pelagic phyto and
zooplankton [24], they consumed more refractory organic
4. Discussion particle in the upper water column and reduced the
quantity and quality of food material reaching the bottom
Biological trait analysis of the benthic foraminiferal water. Food availability was made worse for the bottom-
taxa and trait composition in the tropical Pacific Ocean dwelling taxa as the rise in temperature resulted to
have enabled us to understand faunal turn over and trait increase in the opportunistic taxa (e.g Quadrimorphina
reorganization during the period of extreme climate profunda and Nuttalides truempyi) that out-competed the
conditions associated with the PETM. The changes in trait epifauna and shallow infauna by consuming the limited
composition are consistent with foraminiferal turnover food supply ([48]; Table 4).
during the PETM in all the studied sites. However, our The faunal composition from the raw data at the
result showed that the disappearance of some taxa did not recovery interval demonstrated a period of highest and
immediately affect the change in trait composition and most stable supply of quality nutrients to the sea floor.
hence the ecological functioning performed by them as The highest abundance of the deep infaunal morphogroup,
seen in Site 1209B (Figure 5). Foraminifera reacted by as well as other high organic carbon influx indicators
either increase in the abundance of the taxa that shared across this interval (Figure 6), strongly supports this
similar traits or taxa with cosmopolitan behaviour that can observation. The high nutrient supply during the recovery
tolerate a wide range of ecological changes. In addition, may be attributed to the enhanced continental weathering
the extinction of some trochospiral and macro perforated [49] supplying nutrients to the ocean and a smaller
taxa did not lead to the immediate disappearance of those number of species competing for available resources after
traits (Figure 5) as other taxa reacted by increase in the PETM.
abundance [32] and thereby sustaining the ecological The evaluation of trait composition indicate that the
functioning. The changes in foraminiferal traits were prevailing conditions at the sea floor before the CIE
found in most case to lag behind the taxonomic turnover favoured species with elongate and uniserial test; neck and
(Figure 5). bifid teeth as well as bi/triserial forms [36]. These species
are well adapted to infaunal lifestyle and are
4.1. Changes in Taxa and Trait Compositions predominantly Stilostomellids, Pleurostomellids and
Buliminids. In general, the trait composition that
in Relation to Palaeoecological constituted 50% similarities across the three PETM
Parameters interval show that fine perforation, deep infauna, sessile,
deposit feeder, terminal aperture, hyaline calcite test, bifid
4.1.1. Nutrient Supply in the Pacific Ocean
teeth, elongate, uniserial and shallow infauna and
during the PETM
spherical aperture (Figure 5) were the most significant
Nutrient supply to the benthic zone was inferred from traits during the CIE across the studied section. These
the faunal composition, infaunal/epifaunal ratio, species traits demonstrate high tolerance to high organic carbon
and trait turnover from the statistical analyses. The faunal influx to the bottom ocean and extreme environmental
assemblages in the Pacific Ocean (Sites 1209B and 1212B) conditions [36].
are dominated by calcareous infaunal taxa primarily by Taxa with coarse perforations, trochospiral coiling and
Buliminids, Stilostomellids/Pleurostomellids and Bolivinids. epifaunal habit (e.g. G. beccariformis) was extirpated
These taxa in the modern and ancient oceans thrive in the during the PETM perhaps because they required high
area of high and sustained food supply and low oxygen dissolved oxygen and lowered organic matter to thrive,
[25,39,45,46,47]. The relative dominance of infaunal but high organic matter influx that resulted in bottom
morpho-groups with a coeval high abundance of water anoxia and acidification making the bottom water
Buliminids at the Pacific sites (Table 3 and Table 4; [32]) uninhabitable for them. Foraminifera with traits such as
suggest a significant supply of nutrient to the seafloor elongate cylindrical, flabelliform or biserial architecture
during the PETM. The result from our SIMPER analyses were reported to have high surface to volume ratio that
between the pre-CIE and other intervals showed an enables them to successfully adapt in the infaunal habitat
increase in nutrient flux indicators such as Bulimina with high organic matter inundation and anoxia [46].
kugleri and Bolivina inconspicua (Table 3). The nutrient Additionally, this form of chamber arrangement provides
supply started to decrease within the CIE interval as communication/exchange link at each end and this can
shown by a decrease in the Bulimina taxa (Figure 6). The reduce the rate of protoplasm mixing between the inside
lowering in the number of Buliminids and Stilostomellids and outside of the test leading to decreased metabolic
in the samples across this interval (Figure 6) was an activity within the foraminiferal cell. This anatomy could
indicator of oligotrophy. The abundance of these taxa may reduce oxygen and nutrient requirement of the organism.
not have been extremely affected by carbonate dissolution Excessive organic carbon rain from the upper water
since they live inside the sediment and also very low column may have contributed to the decrease in some less
carbonate dissolution was recorded in the Pacific Ocean competent epifaunal taxa because high abundance of
during the PETM [32]. organic matter in the sea floor hinders pseudopodia
There was an initial increase in the Buliminid function as they are usually overwhelmed by algal growth
abundance at the beginning of the CIE (Figure 6) which [37,47].
 Journal of Ocean Research 15

Figure 6. Changes in foraminiferal composition of major taxa in the Pacific Sites with core depth (mbsf) and foraminifera bound isotope records. The
lithology is mainly foraminiferal oozes. The lithology and δ13C record are those of Takeda and Kaiho (2007) while the morphogroups and taxa curves
were created in this study

4.1.3. Productivity/global Carbon Cycle abundance of both the benthic and planktonic foraminifera
[planktonic foraminiferal data in [50]) as well as the
4.1.3.1. Palaeoproductivity/global Carbon Cycle δ13C signature of the biogenic carbonates supports this
in the Pacific Ocean assertion. The carbon isotope record of the surface-dwelling
Palaeoproductivity in the Pacific Ocean interpreted planktonic foraminifera and bottom-dwelling taxa strongly
from fauna and trait results from sites 1209B and 1212B suggests high primary productivity in the surface ocean
varied across the PETM intervals. The diversity and and significant export production to the seafloor denoting
16 Journal of Ocean Research

efficient benthopelagic coupling. The evidence of high of disparity between food supply and productivity.
export production in the Pacific Ocean was further Trophic focusing involves winnowing of the fine organic
supported by a notable abundance of taxa regarded particle by current and concentrating them on a particular
as a good indicator of high export production such part of the ridge [47,54].
Siphogenerinoides brevispinosa, Stilostomellids and In summary, it may be possible that the initial increase
Buliminids ([47]; Table 3 and Table 4) at Sites 1209B and in the ocean-atmospheric CO2 and the coeval rise in
1212B. temperature before the CIE resulted in an increase in
The productivity at the main CIE section was not very productivity with enhanced organic matter rain to
clear perhaps as a result of massive carbonate dissolution the seafloor but with further rise in temperature,
that led to shoaling of CCD globally during the PETM. phytoplankton productivity optimum was exceeded in the
All the proxies indicate a collapse in both pelagic (surface) surface ocean leading to lowered export production. More
and benthic productivity. The rise in temperature that so, the increased ocean acidification resulted in reduced
resulted from the PETM must have increased the calcification in form of smaller and thinner test walls in
metabolic rate of the pelagic primary producers [19]. The benthic foraminifera and increase in bacterial activity in
high temperature recorded during the peak of the CIE the sea floor. Increase in the opportunistic and resilient
must have caused encystment of many phytoplankton and taxa utilised more bicarbonate in the upper water column
reduced primary production (with episodic productivity and acted as a sink to the CO2. The increase in silicate
when the environment is conducive to reproduce) while weathering from the continents enhanced this process and
the zooplankton may have moved deeper into the water triggered the recovery of PETM. However, export
column and thoroughly foraged all the available organic production to the benthic realm never returned to the
matter and diminished the quality and quantity of organic pre-CIE scenario as suggested by bulk carbonate and
carbon reaching the seafloor. foraminiferal δ13C records in Figure 6.
Enhanced foraging of the upper water column would
mean that less phytodetritus will be reaching the ocean 4.1.3. Oxygen Concentration in the Seafloor
floor resulting in food scarcity and increased competition. in the Equatorial Pacific Ocean
In addition, increase in the solubility of calcium carbonate Estimating the amount of dissolved oxygen in the sea
resulting from higher CO2 concentration and lowered pH floor using faunal association is complicated but has been
in the ocean will stimulate foraminifera to reduce successfully demonstrated by [55]. This is because oxygen
calcification by building smaller and thinner test walls concentration in the bottom water also depends on the
which are less likely to be preserved in the sediment interaction between the quantity of organic matter
record. reaching the seafloor, deep water circulation pattern,
Palaeoproductivity picked up again after the BBE as temperature and faunal composition. Another difficulty
indicated by the increase in the relative abundance of both lies in the fact that some taxa (especially epifauna)
planktonic and benthic foraminifera at Site 1209B [32,50], considered to be abundant at a particular amount of
though this was not reflected on the δ13C record as it oxygen concentration does not spend their whole lifetime
remained relatively low throughout the rest of the studied in a single niche but migrate within a wide range of
interval in the Pacific. The lowering of δ13C record in variable oxygen concentration environment during their
benthic foraminifera even when the abundance of biomass life [39]. Nevertheless, the study by [55] identified critical
increased could be attributed to vital effect. dissolved oxygen concentration markers for estimating the
The connection between trait composition and productivity amount of oxygen available in the benthic ecosystem.
has not been well publicised in foraminiferal research. Foraminiferal composition in the Pacific Ocean (Sites
Reference [39] believed that cylindrical spherical and 1209B and 1212B) indicates low oxygen concentrations
planispiral morphogroups usually with infaunal habit are throughout the PETM. Prior to the initiation of the CIE,
common in the area of high productivity. In the PETM the faunal assemblage was composed of dysoxic
section at the Pacific Ocean, trait composition was (moderate oxygen concentration) indicators characterised
dominated by the terminal apertures, fine perforation, by a mixture of low oxygen taxa such as Bolivina
grazers, infauna, planispiral, elongate test, sessile, biserial- inconspicua, Buliminids and stilostomellids (Table 3) and
triserial and complex apertures (Figure 4). These trait oxic fauna like Gavelinella spp., Anomalinoides and
assemblages strongly support the [39] hypothesis. Another Gyroidinoides species occurring together in the sediment.
possible explanation for the increase in cylindrical and The high abundance of deep infauna, in association
bi-triserial traits may be related to their response function with a few number of epifaunal taxa reveals that oxygen
towards environmental perturbation and not really to level was already low in the benthic environment, but just
productivity increase. Increase in the abundance of slightly enough to keep the species that needed higher
oligotrophic taxa such N. trumpyi, Q. profunda and oxygen concentration on life support. The threshold of
G. subglobosa may suggest lowered productivity or taxa that require high oxygen concentration was probably
well-functioning bentho – pelagic coupling (Benthic – Pelagic reached at the onset of the CIE that resulted in the benthic
coupling refers to the exchange of mass, nutrients/organic foraminiferal extinction (BEE). The BEE may largely
materials or energy between benthic and pelagic habitats have been caused by low oxygen concentration
of the ocean [51]. This is also in line with the deduction because high porosity epifaunal taxa like Gavelinella
on the food supply that suggested sustained mesotrophy beccariformis needed high dissolved oxygen for their
during the PETM in the Pacific Ocean. In addition, the metabolic requirements but could not get enough. Low
topography of elevated platform like the Shatsky Rise amount of dissolved oxygen accompanied by high organic
[52,53], trophic focusing has been identified as the cause carbon influx to the sea floor plus water column
 Journal of Ocean Research 17

stratification combined to exterminate the susceptible foraminiferal census data from [32] revealed a very
(highly perforated) epifaunal species. Other epifaunal dynamic changes in foraminiferal events across the
species that survived this hypoxia are well adapted to low studied sites. However, the foraminiferal trait diagrams in
oxygen concentration and had the ability to tolerate high Figure 6 showed a more uniform and predictable
organic carbon influx or are able to move up and down the bioevents. The similarities in trait events in Figure 6
sediment column. indicate that some foraminiferal traits are redundant
The acme of Bolivina gracilis as well as a significant meaning that different species share similar traits and
increase in the abundance of opportunistic taxa when one goes into extinction similar species sharing the
(Q. profunda) have been interpreted as a marker for low same trait can still maintain ecological functioning in the
oxygen concentration at the peak of the CIE [32]. The ecosystem.
amount of dissolved oxygen slightly increased after the Our results also have shown strong evidence that the
peak of the CIE and at the beginning of the PETM trait composition of foraminifera can be used to
recovery as suggested by high abundance of infaunal taxa characterised climatic events across basins as exemplified
(Buliminids) and the reduction in the opportunistic taxa by trait similarities during the hyperthermal in both basins
([32]; Table 3) because more oxygen was available in the (Figure 6).
sediment and the infauna could favourably compete with The biological traits analysis of foraminiferal turnover
the opportunistic taxa for the accessible nutrients. from the Shatsky Rise (Pacific Ocean) across the
The trait composition from SIMPER results revealed PETM has revealed the ecophenotypic responses of
that the dominant traits driving ecological changes in Sites benthic foraminiferal community to the environmental
1209B and 1212B during the PETM are deep infauna, perturbations. The increase in temperatures and dissolved
sessile, elongate, no ornamentation, fine perforation, inorganic carbon associated with the event resulted in
terminal apertures, planispiral and bi/trispiral test shape enhanced food supply, decreased the amount of dissolved
(Figure 4). These trait assemblages strongly suggest oxygen and palaeoproductivity in the Pacific Ocean. The
adaptation to low oxygen condition, [55] describes the excessive supply of organic material to the seafloor and
morphological characteristics of low oxygen taxa as thin lowered oxygen concentration resulted in the extirpation
wall, elongate, spiral and multi-serial. These attributes of the highly porous trochospirally coiled epifaunal taxa
help them to maximise available oxygen to continue their (Figure 6).
metabolic activities in the face of hypoxia. Elongate and The trait distribution partly conforms to the taxonomic
biserial taxa such as Bolivina have been reported to composition of foraminifera from which they were
respiring nitrate in the absence of oxygen [56]. Some derived (section 4.1), however, the biological trait analysis
species of foraminifera found in the oxygen minimum demonstrated how foraminifera maintained benthic
zone have also been reported to lack ornamentation [37] functioning in the face of an extreme climate event that
and no ornamentation trait was relatively high in the led to the extinction of numerous benthic foraminifera.
SIMPER result as shown in Figure 4. There was a mixture For instance, the extinction of taxa with highly calcified
of traits like basal interiomarginal, trochospiral, and and mega perforated taxa like Gavellinidae at the Shatsky
species with umbilical apertures. Such traits are indicating Rise was followed by an increase in smaller-sized
an increase in the abundance of opportunistic taxa across opportunistic taxa such as Q. profunda; (Table 3) with
PETM events and suggest environmental disturbance or micro-perforated tests that require less dissolved oxygen
periods of episodic bloom as a result of a seasonal and well adapted to high organic rain.
increase in oxygen concentration. The result from statistical analyses showed that infaunal,
sessile life habits, cylindrical elongate and bi-triserial test
forms, complex terminal apertures and omnivorous
5. Conclusions feeding modes were the most resilient traits during the
hyperthermal (Figure 5).
This study is a novel one, and it pioneered the Along with other opportunistic taxa the Buliminids,
utilisation of trait changes in fossil foraminifera as indices Bolivinids, Pleurostomellids and Stilostomellids may have
for paleoecological changes in the benthic system. We utilised their facultative anaerobic metabolism enhanced
have shown that trait composition in conjunction with by cytoplasmic streaming to sustain calcification and drew
faunal assemblages can be used as indices for palaeoecological down the excess dissolved inorganic carbon in the water
changes and to detect ecological disturbance in the marine column. Increase in populations of foraminifera during
ecosystem. Detail examination of foraminiferal traits across the recovery intervals in all the studied sites together
the PETM sections at Northeastern Pacific indicated that with high-temperature feedbacks such as increase in
mostly heavily calcified and perforated benthic foraminiferal precipitation and silicate weathering would have
taxa went into extinction during the PETM but a eventually returned the ocean to its normal state.
significant number survived. This suggests that foraminifera
could tolerate a wide range of ecological changes and
withstand extreme ecological conditions through various Acknowledgements
trait manoeuvring such as increasing the abundance of
taxa with resilient traits during environmental perturbation. We acknowledge the authors of Takeda and Kaiho,
The results from this study also showed that changes in 2007 from whose benthic foraminiferal census data we
foraminiferal traits do not occur at the same time as the used to generate the trait composition of foraminifera for
faunal turn-over in foraminiferal taxa, implying that traits this study. Ebonyi State Government, Nigeria and School
of foraminifera are conserved. Careful examination of
18 Journal of Ocean Research

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