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Marine Micropaleontology 76 (2010) 67–75
Contents lists available at ScienceDirect
Marine Micropaleontology
j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / m a r m i c r o
Research paper
Benthic foraminiferal responses to absence of fresh phytodetritus:
A two-year experiment
Elisabeth Alve ⁎
Department of Geosciences, University of Oslo, P.O. Box 1047 Blindern, 0316 Oslo, Norway
a r t i c l e
i n f o
Article history:
Received 3 February 2010
Received in revised form 26 May 2010
Accepted 31 May 2010
Keywords:
Survival
Benthic foraminifera
Food quality
Trophic strategy
Refractory organic material
Resilience
a b s t r a c t
Sediment and bottom water from 320 m water depth in the Skagerrak basin (NE North Sea) was maintained
in the laboratory and kept unfed in the dark, at ambient temperature, for two years. Although the relative
abundance of agglutinated taxa in the sediments increased at the expense of allogromiids and calcareous
forms, the deprivation of fresh phytodetritus caused only a moderate change of the faunal composition of the
bathyal, benthic foraminiferal assemblage (six of the seven most abundant species were the same before and
after the treatment; overall similarity was 58%). Among the most common species, the halt in supply of fresh
organic material promoted population growth in some (e.g., Textularia earlandi, Leptohalysis gracilis, Melonis
barleeanum), some maintained their populations (e.g., Globobulimina auriculata, Liebusella goësi, Eggerelloides
medius), while others (e.g., Nonionella iridea, Cassidulina laevigata, and some allogromiids, particularly
Micrometula hyalostriata) nearly disappeared. The different responses probably reflect the species' relative
dependence on fresh phytodetritus. Those species which could utilize food stored or produced in the
sediments (e.g., bacteria and degradation products) increased or maintained their populations, whereas
those dependent on fresh phytodetritus and/or associated early-decomposition products declined. In spite of
these changes, the species diversity showed only a minor reduction. The overall moderate response to lack of
fresh phytodetritus was probably due to the fact that the assemblage already was adapted to an environment
dominated by poor quality food particles. The study illustrates that the quality of organic material has an
important impact on the composition and maintenance of some benthic foraminiferal communities, that the
faunal response to reduction, or even a halt, in the supply of fresh phytodetritus, is not necessarily immediate
or dramatic, and that the response depends on the trophic conditions prevailing in the area when the halt
occurs.
© 2010 Elsevier B.V. All rights reserved.
1. Introduction
An understanding of the dynamics and processes controlling the
spatial distribution and microhabitats of benthic foraminifera is crucial
for optimizing palaeoecological interpretations of both older and more
recently deposited fossil assemblages. Due to an increased realization
of the role they play in recycling of organic carbon and their usefulness
as palaeoenvironmental and human impact indicators, the last
decades have seen an increasing number of studies focusing on
relationships between Corg-fluxes and benthic foraminiferal ecology.
Shirayama (1984) and Corliss and Emerson (1990) illustrated some of
the fundamental relationships between the flux of Corg to the sea floor,
dissolved [O2] of the benthic habitat and meiofauna/benthic foraminiferal microhabitats. Their thoughts and suggestions were synthesised into the TROX model (Jorissen et al., 1995). Since then, numerous
studies have extended our knowledge on aspects of microhabitats,
⁎ Tel.: + 47 22857333; fax: + 47 22854215.
E-mail address: ealve@geo.uio.no.
0377-8398/$ – see front matter © 2010 Elsevier B.V. All rights reserved.
doi:10.1016/j.marmicro.2010.05.003
trophic status, and associated environmental parameters. It is now
well established that benthic foraminifera in oligotrophic environments, such as the deep sea, respond to phytoplankton blooms and
subsequent arrival of phytodetritus at the sea floor by increased
abundance of opportunistic species (e.g., Gooday, 2003). Responses
are also seen in shelf (e.g., Duchemin et al., 2008) and coastal/fjordic
(e.g., Gustafsson and Nordberg, 2001) environments where food is a
limiting factor.
Phytodetritus deposition in the oceans is highly variable spatially
and temporally. For example, some regions may not have phytodetritus accumulation on the sea floor each year (Beaulieu, 2002).
Recently, environmental remediation in areas previously impacted by
cultural eutrophication experience reduced primary production and
hence less food to the benthos (e.g., Alve et al., 2009). It would be
useful to understand the impact this variability has on benthic
foraminiferal faunas. How does a decrease or even a cease in
phytoplankton production, and thereby a depletion in the flux of
freshly produced organic material to the sea floor, affect the benthic
fauna? Answers to this question can throw light on how dependent
certain species are on regular supplies of fresh organic material. The
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68
E. Alve / Marine Micropaleontology 76 (2010) 67–75
Table 1
Number of live (stained) foraminifera counted in the freshly collected 2002- and the stored 2004-sediments. The two size fractions and their sums are shown separately for each data set.
Data-set
Size fraction counted
2002
63–125 μm
2002
N 125 μm
2002
N 63 μm
2004
63–125 μm
2004
N 125 μm
2004
N 63 μm
Allogromia crystallifera
Cylindrogullmia alba
Gloiogullmia sp.
Micrometula hyalostriata
Nemogullmia longevariabilis
Tinogullmia hyalina
Allogromiid sp N2
Allogromiid “oval”
Allogromiid “neck”
Adercotryma wrighti
Astrammina sp. (fragile)
Bathysiphon argenteus
Bathysiphon sp.
Cribrostomoides crassimargo
Cribrostomoides jeffreysii
Cribrostomoides subglobosa
Eggerella europeum
Eggerelloides medius
Haplophragmoides bradyi
H. cf. membranaceum
Hippocrepinella alba
Hippocrepinella remanei
Leptohalysis catenata
Leptohalysis gracilis
Leptohalysis scottii
Leptohalysis sp.
Liebusella goësi
Morulaeplecta bulbosa
Paratrochammina sp.
Phainogullmia spp.
Portatrochammina murrayi
Recurvoides trochamminiforme
Reophax dentaliniformis
Reophax fusiformis
Reophax rostrata
Reophax subfusiformis
Saccammina (white, fine grained)
silver saccaminid
Technitella sp.
Textularia kattegatensis
Textularia earlandi
Trochammina “skrumpa”
Trochamminopsis quadriloba
trochamminid
trochamminid
Bolivinellina pseudopunctata
Brizalina spathulata
Bulimina marginata
Cassidulina laevigata
Elphidium albiumbilicatum
Elphidium excavatum
Epistominella vitrea
Fissurina sp.
Gavelinopsis praegeri
Globobulimina auriculata
Hopkinsina pacifica
Hyalinea balthica
Lenticulina sp
Melonis barleeanum
Nonionella turgida
Nonionella auricula
Nonionella iridea
Oolina hexagona
Pullenia osloensis
Quinqueloculina sp.
Stainforthia concava
Stainforthia fusiformis
Uvigerina peregrina
No. counted foraminifera
No. spp
Allogromiid taxa (%)
Agglutinated taxa (%)
Calcareous taxa (%)
Fisher alpha index
ES(100)
3
22
28
113
28
11
19
3
12
4
0
0
1
0
2
0
4
65
0
1
6
0
0
16
11
2
0
1
0
24
15
0
2
48
0
0
3
1
0
11
254
5
0
2
0
27
1
2
1
0
0
2
3
0
5
0
1
2
0
0
2
36
0
87
2
1
233
0
1132
46
21
43
36
9,6
22
4
4
1
4
1
0
2
0
0
0
0
0
0
1
0
3
0
98
6
0
0
0
0
0
1
0
322
0
0
1
7
2
0
1
4
3
5
0
0
0
0
0
3
0
2
0
1
1
30
0
1
0
0
0
347
0
4
0
9
3
0
0
0
3
0
0
1
4
879
32
2
52
46
6,5
12
7
26
29
117
29
11
21
3
12
4
0
0
1
1
2
3
4
163
6
1
6
0
0
16
12
2
322
1
0
25
22
2
2
49
4
3
8
1
0
11
254
5
3
2
2
27
2
3
31
0
1
2
3
0
352
0
5
2
9
3
2
36
0
90
2
1
234
4
2011
59
13
47
40
11,4
23
0
0
2
6
4
0
0
0
1
21
0
6
0
0
0
0
35
40
20
0
24
2
2
108
3
0
2
1
3
6
8
0
0
17
6
0
1
0
20
0
344
25
1
0
0
21
0
1
0
0
0
0
0
1
4
11
0
0
13
1
0
3
0
92
0
0
104
0
959
36
1
72
26
7,4
19
0
0
0
0
1
0
0
0
0
1
0
2
0
0
0
0
0
35
0
0
11
4
0
2
0
0
98
0
0
0
0
0
0
3
12
1
1
0
4
0
0
0
2
0
0
0
0
0
1
1
0
0
0
0
127
0
0
0
8
1
0
0
0
0
0
0
1
0
316
20
0
56
44
4,7
12
0
0
2
6
5
0
0
0
1
22
0
8
0
0
0
0
35
75
20
0
35
6
2
110
3
0
100
1
3
6
8
0
0
20
18
1
2
0
24
0
344
25
3
0
0
21
0
1
1
1
0
0
0
1
131
11
0
0
21
2
0
3
0
92
0
0
105
0
1275
39
1
68
31
7,6
21
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E. Alve / Marine Micropaleontology 76 (2010) 67–75
69
Table 1 (continued)
Data-set
Size fraction counted
H′(loge)
H′(log2)
No. of Gromia pr counted foraminifera
No. Gromia/No. foraminifera
2002
63–125 μm
2,7
3,8
9
0,01
2002
N 125 μm
2002
N 63 μm
2004
63–125 μm
2004
N 125 μm
1,6
2,3
87
0,10
2,8
4,0
96
0,048
2,4
3,5
1
0,00
1,7
2,5
23
0,07
results may have important implications for 1) understanding the
processes (including the time aspect) associated with environmental
remediation and faunal recovery following human impacts on benthic
ecosystems (e.g., reduced nutrient discharges), 2) interpretations of
what consequences e.g., extraterrestrial impacts with subsequent loss
of primary production, may have on an important part of the benthic
community, and 3) understanding variations in benthic foraminiferal
13
δ C.
This study addresses the effect of phytoplankton deposition
variability by maintaining benthic foraminifera in the laboratory
without the introduction of new food over a two-year period. A
comparison of the living fauna after two years with living fauna
analysed at the time of sediment collection provides insight into the
impact of phytodetritus and the resilience of benthic foraminifera to
food availability. The same sediment was also used in an experiment
focussing on survival and dispersal potential of benthic foraminiferal
propagules (Alve and Goldstein, 2010).
2004
N 63 μm
2,6
3,8
24
0,02
35.2–35.3, and temperature 7.0–7.4 °C (data from sta. H1–H3 in Ståhl
et al., 2004).
On 21st August, 2002, sediment from three of the six containers
was combined and sieved with ambient sea water through 32, 63, and
125 μm sieves, and the b32 μm-fraction was used in a propagule
experiment (Alve and Goldstein, 2010). The coarser fractions were
fixed in 4% buffered formalin in sea water, later re-sieved, and
preserved in 70% ethanol with rose Bengal (1 g/L). Parts of the 63–
125- and N125 μm-fractions were examined for the propagule study.
The sediment in the remaining three containers (sediment height
about 1.5 cm in each) was stored untouched (sealed at all times) in a
dark cold-room (7 °C) for two years. On 27th August, 2004, the stored
sediment was sieved through the same set of sieves, the fine fraction
(b32 μm) was used in the propagule experiment (Alve and Goldstein,
2010), and the coarse fractions fixed and treated as described above.
In the present study, the rose Bengal-stained 63–125- and N125 μmfractions were combined and subsamples of the N63-μm fraction of the
2002- and 2004-sediments were sieved through 63- and 125-μm sieves.
2. Material and methods
Sediment used in this study was collected with a box corer on 12th
August, 2002, from a 320-m site in the Skagerrak basin (North Sea),
midway between Norway, Sweden and Denmark (58° 07.90′N; 9°
54.00′E). Immediately upon arrival on deck of the RV Arne Tisselius, 9 L
of seawater just above the sediment–water interface in the box corer
were transferred to a plastic container, and 29 cm × 26 cm of the
surface sediment (top 2 cm) was randomly transferred to 6
transparent 1000 mL (Joni DK, no. 50300001) plastic containers
(sediment height 1–1.5 cm in each), ambient sea water was added
and the containers were sealed. The containers were kept in dark
cold-rooms at ambient temperatures, first on the ship (5 °C) and later
at Oslo University (7 °C). Bottom water characteristics of the present
sampling site include bottom water [O2] N85% saturation, salinity
Fig. 1. Relative abundance of the most common species (N63-μm fraction) at a 320-m
site in the middle part of the Skagerrak at the time of collection in 2002 (left) and from
the same site and collection after having been kept in the original sediments for two
years in the dark, in closed containers with ambient seawater and at ambient
temperature (right).
Fig. 2. Relative abundance of the most common species (N63-μm fraction) at a 320-m
site in the middle part of the Skagerrak at the time of collection in 2002 and from the
same site and collection after having been kept in the original sediments for two years
in the dark, in closed containers with ambient seawater and at ambient temperature.
Solid line (lower diagram) shows the 1:1 relationship between the two datasets.
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70
E. Alve / Marine Micropaleontology 76 (2010) 67–75
2002- and 2004-sediment yielded abundant populations of several
species with individuals N63 μm in size after being exposed to simulated
shallow-water conditions (Alve and Goldstein, 2010). Because figures
for the exact volume of the original 2002-sediment and of the stored
2004-sediment were not needed for the propagule dispersal experiment, absolute abundance data (foraminifera/cm3) were not possible to
determine for the present study. Species diversity was expressed using
the Fisher alpha (Fisher et al., 1943), Shannon–Wiener (Shannon and
Weaver, 1963) with H′(loge) and H′(log2), and Hurlbert's (Hurlbert,
1971) ESn = 100 indices. The similarity between pairs of samples was
calculated according to Walton (1964) by summarizing the lowest
common percentage values for each species.
3. Results
Fig. 3. Relative abundance of the most common species (top: 63–125-μm- and
bottom: N125-μm fractions) at a 320-m site in the middle part of the Skagerrak at the
time of collection in 2002 (left) and from the same site and collection after having
been kept in the original sediments for two years in the dark, in closed containers with
ambient seawater and at ambient temperature (right). For relative abundance of the
same species in the complete N63-μm fractions, see Fig. 1.
The complete content of live (stained) foraminifera in the 63–125 and N
125-μm fractions was wet-counted. Only individuals with brightly
stained cytoplasm in most chambers were considered as being live at
the time of collection. The presence of live populations was confirmed
through the propagule experiment as the b32 μm-fraction of both the
Table 2
Categories of bathyal (320 m) species according to how their relative abundance
changed during two years of isolation (unfed) in the dark (i.e., deprived of fresh
phytodetritus) in their native sediment with ambient water and at ambient
temperature. %-values refer to the N63 μm-fractions.
Category 1
Category 2
Common taxa which
nearly disappeared
Taxa increasing from rare
Abundant taxa showing
(b 0.5%) to common (2–9%) some change
Leptohalysis gracilis
Allogromiids
Eggerella europeum
Nonionella iridea
Cassidulina laevigata Hippocrepinella alba
Trochammina “skrumpa”
Technitella sp.
Melonis barleeanum
Adercotryma wrighti
Haplophragmoides bradyi
Reophax rostrata
Category 3
Textularia earlandi (++)
Globobulimina auriculata (−)
Liebusella goësi (−)
Stainforthia fusiformis (−)
Eggerelloides medius (−)
Pullenia osloensis (+)
Reophax fusiformis (−)
The 2002 sub-sample yielded 2011 live (stained) individuals; 1132
in the 63–125-μm- and 879 in the N125-μm fraction (Table 1). The
most abundant taxa in the complete N63-μm fraction of the 2002assemblage were Globobulimina auriculata (18%), Liebusella goësi
(16%), allogromiids (13% including 6% Micrometula hyalostriata),
Textularia earlandi (13%), and Stainforthia fusiformis (12%), with
Eggerelloides medius, Pullenia osloensis, Reophax fusiformis, Nonionella
iridea, and Cassidulina laevigata as common (8–2%) species (Figs. 1
and 2). When considering the two size fraction separately, G.
auriculata and L. goësi strongly dominated the larger (N125 μm),
whereas allogromiids, T. earlandi, and S. fusiformis dominated the
smaller (b63 μm) fraction (Fig. 3).
After two years, the stored 2004-sediment had a light gray colour
(i.e., no sign of sulphides), and two of the three containers had
polychaete tubes protruding up into the overlying water. Live
(moving) polychaetes and bivalves were present. The foraminiferal
sub-sample had 1275 live (stained) individuals of which 959 occurred
in the 63–125-μm fraction and 316 occurred in the N125-μm fraction.
The most common taxa (N2%) either in the 2002- or in the 2004assemblage, or in both, are grouped into three categories according to
relative abundance (Table 2). Category 1 includes allogromiids, N.
iridea, and C. laevigata which nearly had disappeared by 2004
(Table 1). Category 3 includes all other taxa which were abundant
both in the 2002- and the 2004 assemblage. T. earlandi made up 27% of
the complete N63-μm fraction and 36% of the 63–125-μm fraction in
the 2004 data-set. For G. auriculata, the abundance in the complete
N63-μm fraction was 10%. Its abundance in the N125-μm fraction was
the same as in the 2002-data-set (40%). Category 2 includes
Leptohalysis gracilis, Eggerella europeum, Hippocrepinella alba, Trochammina “skrumpa”, Technitella sp., Melonis barleeanum, Adercotryma wrighti, and Haplophragmoides bradyi, all of which were only
recorded with a few individuals in the 2002-assemblage but were
common (2–9%) in 2004.
The seven commonest species made up 76% of the complete
(N63 μm) assemblage in both the 2002- and in the 2004 data-set. Of
these seven, they had six in common whereas the 7th was M.
hyalostriata in 2002 and L. gracilis in 2004. The similarity in species
composition between the complete (N63 μm) 2002- and 2004assemblages was 58%. For the sub-fractions, the similarity between
the two smaller (63–125 μm) was 56%, whereas that for the larger
(N125 μm) was 85%. In the 2002-assemblage, the smaller fraction
made up 56% of the assemblage whereas in 2004, the figure had
increased to 75%. The 2002–assemblage had 59 species of which 31
were recorded in the stored 2004-assemblage. An additional 8 species
were recorded in the latter. Both the 2002- and 2004- assemblages
were dominated by agglutinated taxa but with a higher relative
abundance in the latter. Allogromiids made up 13% and 1% of the
complete (N63 μm) assemblages respectively. The species diversity
indices showed a minor reduction from 2002 to 2004, irrespective of
which index was considered, whereas the relative abundance of
agglutinated forms increased by about 20% (Table 1).
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E. Alve / Marine Micropaleontology 76 (2010) 67–75
The organic-walled rhizarian protist Gromia which is related to the
foraminifera was present in both size fractions of both data sets but its
abundance relative to the number of foraminifera was more than
halved during the two years storage in the dark (Table 1).
4. Discussion
4.1. The culture conditions
During two years storage at ambient temperature, no nutrients
were added to the cultures and the sediment was exposed to indoor
light only for a few minutes per month when items were placed in or
collected from the cold-room. This was probably not enough to trigger
growth or maintenance of algae (Bente Edvardsen and Wenche
Eikrem, pers. com., 2009). A methodological weakness was that no
environmental parameters (except temperature) were measured or
analysed during the two year period. However, it is likely that the
salinity remained constant as the cultures were sealed at all times and
the following suggests stable geochemical conditions during the
course of the experiment. During the two year storage, bioturbation
within the thin sediment-layer (e.g., Hemleben and Kitazato, 1995;
Gross, 2002) and oxygen penetration through the culture walls
probably prevented the 1–1.5-cm thin sediment layers from turning
anoxic. Macrofauna was present and there were no signs of sulphide.
Lack of deep infaunal space cannot have served as a serious limiting
factor as species of Globobulimina (abundant in the present study) are
commonly among the deepest recorded infaunal foraminiferal species
(e.g., Corliss and Van Weering, 1993; Fontanier et al., 2002).
4.2. Species responses to absence of freshly produced algae
The only food available for the foraminifera during the two years in
isolation was food particles already present in the sediment at the
time of collection and associated bacteria and degradation products.
Still, of the 59 species recorded in the original 2002 assemblage, at
least 31 survived and most taxa which were abundant in 2002 were
still abundant in 2004 (Fig. 1). Also, the fact that six of the seven most
abundant species in 2002 were still the most abundant two years
later, show that no dramatic faunal restructuring occurred. Similarity
indices and changes in relative abundance of the smaller vs the larger
size fraction (Fig. 3) indicate that the faunal response primarily
occurred in the smaller species. This moderate response is in contrast
to the dramatic faunal change that occurred with the assemblage in
the same sediment when the fine fractions containing juveniles only
were exposed to simulated shallow-water conditions (Alve and
Goldstein, 2010).
The most pronounced negative faunal change was seen in the
Category 1-species (Table 2) with a strongly reduced relative abundance
of the organic-walled allogromiids and a near disappearance of the
calcareous N. iridea and C. laevigata (Figs. 2 and 3). The present results
are in accordance with the view that these two calcareous species and at
least some allogromiids are shallow infaunal taxa, linked to the presence
of phytodetritus (possibly different kinds) on the sea floor (e.g., Corliss
and van Weering, 1993; Gooday and Hughes, 2002; Gross, 2002;
Duchemin et al., 2008). For allogromiids, their relative abundance in the
2002-assemblage is within the range reported for deep-sea assemblages
(e.g., Gooday, 1986; Gooday and Hughes, 2002). It seems, in general,
that they are less responsive to inputs of fresh organic material than
calcareous foraminifera (Gooday, 2002). On the other hand, a species of
Tinogullmia (T. riemanni) is a phytoplankton-dwelling form but also
occurs in the sediment below (Cornelius and Gooday, 2004). Further,
while some hard-shelled species were recorded living down to 30 cm
below a marsh surface, allogromiids lived exclusively at the surface
(Goldstein et al., 1995).
Fatty acid biomarker analyses have shown that another Cassidulina
species, C. crassa, feeds selectively on the high quality part of freshly
71
deposited organic matter from phytoplankton bloom events (Suhr and
Pond, 2006) and N. iridea seems able to “withstand relatively low
background organic flux but needs pulsed arrivals of phytodetritus in
order to dominate the assemblage” (Duchemin et al., 2005, p. 213). The
present results show that most Category 1 taxa, although reduced in
abundance, can survive for a longer time (here, two years) than the
months “normally” needed between phytoplankton blooms (for
survival of deep-sea cultures, see also Hemleben and Kitazato, 1995).
There are two potential explanations: 1) that they can survive for at least
two years by reducing their metabolism. The quality of settling organic
particles is a key factor in understanding temporal variability in benthic
metabolic rates (Ståhl et al., 2004); 2) that they can survive on degraded
organic material or on bacteria associated with phytodetritus (rather
than on the phytodetritus itself) as suggested for Cassidulina teretis
(Gooday and Lambshead, 1989), i.e., they have a potentially varied diet.
The latter is supported by the fact that the cytoplasm of live C. laevigata
may have bright green, orange, shades of brown, or cream colours (Alve
unpubl. observations) indicating that it ingests other food items as well
as chloroplasts. Species of Allogromia used their pseudopodial networks
to harvest bacterial biofilm parcels (Bernhard and Bowser, 1992).
A positive response pattern was seen in the Category 2-species
(Table 2) for most of which the trophic strategies are not well known. T.
earlandi stands out as it became the predominant species (Figs. 1 and 2)
following the two years isolation treatment. In addition to the present
findings, there are several indications that T. earlandi is an omnivorous
opportunist able to feed on and reproduce in response to a wide
spectrum of food resources: 1) it grew and reproduced in high numbers
when exposed to simulated shallow-water conditions (probably in
response to algae and/or bacteria growing when exposed to sun light)
following two years of dark isolation (Alve and Goldstein, 2010), 2) it
suddenly occurred in large numbers in an oil-treated mesocosm
experiment (Ernst et al., 2006), 3) it was one of the predominant
species in terrestrial dominated (C:N ratios N30) sediments deposited
from turbid melt water in an Alaskan fjord (Ullrich et al., 2009), and 4) it
(as Spiroplectinella earlandi) suddenly became the dominant species in
an unfed culture (Heinz et al., 2002).
Leptohalysis is recorded in organic rich, oxygen-limited sediments
influenced by terrestrial plant debris (e.g., Blais-Stevens and Patterson, 1998; discussion in Murray et al., 2003) and Gooday (1996)
suggested that Leptohalysis benefitted from degraded phytodetritus
or from the associated bacterial populations. Both deep-sea and
shallow-water species have been shown to feed on bacteria by deposit
feeding and ingestion of bacterial cells (Goldstein and Corliss, 1994).
Haplophragmoides bradyi is described as an infaunal species
(Gooday 1986), probably implying that it can feed on degradation
products as also indicated by the present study. In the Adriatic Sea,
Adercotryma wrighti (as A. glomeratum) showed a well-defined
subsurface microhabitat as well as a more surficial one (deStigter et
al., 1998). Adercotryma glomeratum has been described as a species
responding positively to phytodetritus (e.g., Gooday, 1988; Heinz et
al., 2002; Koho et al., 2008). However, in the deep sea, although a few
individuals of A. glomeratum occurred in the phytodetritus, most were
recorded in the sediment below (Cornelius and Gooday, 2004).
Whether A. wrighti and A. glomeratum have similar feeding strategies
is not known. As for Technitella, it seems that Technitella melo was the
first benthic foraminifer to colonize a turbidite deposited in the Bay of
Biscay, France, in 1999 and that it took advantage of the foodimpoverished conditions in the days following a turbidite deposition
(Anschutz et al., 2002). Melonis barleeanum was the only calcareous
species in Category 2. A feeding strategy not dependent on regular
supply of fresh organic material, as suggested by this finding, also fits
with the characterization of this species as a typical infaunal species
which does not move up towards the sediment surface following
phytodetritus deposition (Koho et al., 2008).
The fact that all Category 2-species, except one, are agglutinated
support Koho et al.'s (2008) suggestions that calcareous foraminifera
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are more sensitive (i.e., respond positively) than agglutinated forms to
labile organic matter input, that calcareous taxa require a high quality
food source to survive (in the present case some calcareous forms
survived for two years), and that agglutinated species in general
appear to be less influenced by the lability of phytodetritus, and may
have developed other feeding strategies.
The Category 3-species were abundant during two years of unfed
treatment. Among the most abundant ones, G. auriculata and L. goësi
commonly occupy deep infaunal microhabitats in meso-eutrophic
environments (e.g., Corliss and van Weering, 1993; deStigter et al.,
1998; Fontanier et al., 2003; Bubenschikova et al., 2008; Hess and
Jorissen, 2009) and species of Globobulimina seem to be able to feed
on low quality organic matter (Rathburn and Corliss, 1994; Licari and
Mackensen, 2005) as well as fresh phytodetritus (see discussion in
Nomaki et al., 2006). Accordingly, Koho et al. (2008) observed that L.
goësi (as Bigenerina cylindrica) did not move up towards the sediment
surface following phytodetritus deposition, whereas individuals of
Globobulimina affinis are reported to migrate up to ingest algae
(Nomaki et al., 2005). On the other hand, a simulated phytodetritus
sedimentation event revealed almost no response in G. turgida
(Sweetman et al., 2009). Feeding in Globobulimina pacifica includes
small parcels of sediment and organic detritus and it does not seem to
ingest diatoms (Goldstein and Corliss, 1994). The fact that G.
auriculata and L. goësi predominated the N125-μm fraction in both
data sets (Fig. 3) indicates that they are not dependent on the
presence of fresh organic material for survival and that they probably
maintained their populations by feeding on refractory and associated
organic material already present in the sediment. However, they
maintained their populations for two years but did not seem to
reproduce (hardly any small individuals of these species were
recorded). Of other Category 3 species, S. fusiformis is known to
increase its population by a factor of 7 within a month, probably in
response to a spring phytoplankton bloom (Gustafsson and Nordberg,
2001). In the present study, the fact that its relative abundance did not
decline dramatically when deprived of fresh organic phytodetritus for
two years, shows that it is highly capable of maintaining its population
by utilizing other, more refractory food resources or degradation
products and associated bacteria. A varied diet fits well with its
opportunistic life strategy (Alve, 2003) and strongly variable
microhabitat (e.g., Collison, 1980; Alve and Bernhard, 1995; Wollenburg and Mackensen, 1998). A varied diet is probably also characteristic of E. medius, P. osloensis, and R. fusiformis.
4.3. Community response and trophic structure
It is now commonly realized that the flux of organic carbon to the
sea floor is important for the structuring and abundance of benthic
foraminiferal assemblages. In what form (i.e., composition and
nutritional quality of the organic material) the Corg reaches the
benthos has often received less attention (discussion in Murray,
2006). Exceptions include controlled laboratory protocols, ultrastructural evidence etc (for review, see Goldstein, 1999) and in recent
years, efforts using lipids and labelled food (e.g., Nomaki et al., 2006;
Suhr and Pond, 2006; Suhr et al., 2008; Sweetman et al., 2009) have
contributed new insight. This is important because environments
with similar organic loading may contain organic matter with widely
varying degradability and therefore different food value for benthic
organisms (Dauwe and Middelburg, 1998). Along the same line,
several studies have illustrated that sediment organic carbon content
is a weak proxy for food availability (e.g., Alve and Murray, 1997;
Levin and Gage, 1998) and we still have limited direct proofs for
exactly what the different species eat. Fortunately, there is now a
growing body of literature focusing specifically on foraminiferal diets.
In the present study, depriving a bathyal Skagerrak slope
assemblage of freshly produced algae for two years only caused a
moderate change in the faunal composition. Why was the faunal
response not more severe? The faunal composition of the original
2002 data-set agrees well with, and extends in an eastward direction,
the distribution of the live (stained) G. auriculata-assemblage
previously recorded at about 250 to N500 m water depth on parts of
the Skagerrak basin slopes (Alve and Murray, 1995, 1997). Furthermore, it is well documented that the Skagerrak basin (max depth
700 m) is the major sink for particles produced and resuspended in
the North Sea and that the particulate organic material deposited is
highly refractory (e.g., van Weering et al., 1993; Dauwe and
Middelburg, 1998; Dauwe et al., 1998; Kröncke et al., 2004). Bottom
current- and turbidity measurements indicate a significant lateral
transport of suspended particulate matter in the area (Ståhl et al.,
2004). At a 280-m station just north of the present sampling site, high
input of refractory organic matter yields sediments with 2% total
organic carbon content but of low quality (Dauwe et al., 1998). The
sediments support a rich, deeply penetrating macrofauna (down to
20 cm) consisting mainly of subsurface deposit feeding animals that
are generally adapted to poor food sources. As discussed above, most
species in the G. auriculata-assemblage also seem to be able to feed on
refractory and associated organic material, illustrating that both the
macrofauna and at least the foraminiferal part of the meiofauna reflect
the low quality trophic conditions of the habitat. The initial (2002)
low abundance of Category 1 species (Table 2, Fig. 3) probably reflects
that the relative supply of labile, easily metabolisable organic material
to the site is limited, whereas the relative abundance of Category 2
and 3 species reflects a dominance of the more refractory component.
The moderate reduction in species diversity (Table 1) over the two
years period probably also reflects that overall, sustainment of the
Globobulimina-assemblage does not depend on seasonal supply of
fresh phytodetritus. In other words, except for loss/reduction of
“phytodetritus”- species, the food sources (including degradation
products and bacteria) associated with the refractory material stored
in the sediments, seemed able to maintain the overall community
structure. Consequently, because the fauna already was adapted to a
diet dominated by low quality refractory organic material, a halt in the
supply of fresh organic material did not have a profound effect. Still,
the number of species present indicates that the available diet is more
diverse than we so far are able to prove.
Predatory behaviour or symbiosis with chemoautotrophic bacteria
may fulfill some nutritional needs in refractory sediment (Dauwe
et al., 1998). Carnivory is rarely described in benthic foraminifera. One
example is Floresina amphiphaga which is predatory on Amphistegina
gibbosa (Hallock and Talge, 1994), and some other examples made
Suhr et al. (2008) speculate that carnivory may be more prevalent
among foraminifera than previously believed. Whether carnivory is a
trophic strategy among some of the present species is left to be seen.
Overall, the present study demonstrates how a sedimentary
environment dominated by accumulation of refractory organic
material (i.e., low quality food) supports a benthic foraminiferal
assemblage with a trophic structure that can survive for at least two
years without supply of fresh, high quality organic material from the
surface waters. The results indicate that in areas dominated by
refractory organic material, there is a time lag in the benthic response
to reduced organic carbon fluxes. This delayed response probably
occurs because it takes time (depending on sediment accumulation
rates and biogeochemical pore-water conditions) for organic matter
already incorporated in the sediments to degrade/mineralize, leaving
the fauna with adequate food for some time (in the present case
2 years) after the supply has ceased. Although the experimental
conditions represent an extreme situation which probably hardly
occur in nature (perhaps in response to extra terrestrial impacts
which may cause collapse of primary production), the approach aids
the understanding of more general processes and responses. For
example, the present findings have implications for our understanding of processes associated with environmental remediation and
faunal recovery following periods of human impact on benthic
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E. Alve / Marine Micropaleontology 76 (2010) 67–75
ecosystems (e.g., reduced discharge of nutrients and thereby reduced
eutrophication). Finally, the experimental approach (preferably
including a better control of environmental parameters) seems to
have the potential to further explore how dependant benthic
foraminifera are on export production, and thereby the flux of fresh
organic material to the sea floor, i.e., how they respond if the flux is
strongly reduced or ceases for shorter or longer time periods than
demonstrated here.
4.4. Palaeoecological implications
In the fossil record, evidence for changes in oceanic primary
production has been sought by considering changes in the relative
abundance of epifaunal and infaunal forms. Epifaunal taxa are thought
to be indicative of oligotrophic, well oxygenated conditions, and the
dominance of infaunal taxa are considered indicative of increased
primary production and sometimes oxygen depleted conditions. An
example is the Cretaceous/Palaeogene boundary. Although no major
extinctions of benthic foraminifera have been reported for this
boundary, several studies have documented faunal restructuring of
their assemblages across it. This has mainly been explained by a
collapse of oceanic primary production or collapse of the “biological
pump” transporting food to the benthos, whereas more recent studies
argue that the food supply to the deep sea in the Pacific Ocean
increased rather than decreased (discussions in Culver, 2003; Thomas,
2007; Alegret and Thomas, 2009, and references therein). The present
results show that if a bathyal assemblage living in an environment
dominated by refractory organic material experiences a reduction, or
even a halt, in the supply of fresh phytodetritus, the faunal response is
not necessarily immediate or dramatic. The response depends on the
trophic conditions prevailing in the area when the halt occurs, i.e.,
how sensitive the fauna in focus is to the halt. Also, in the present case,
the halt in export production did not reduce the relative abundance of
typical deep infaunal species such as G. auriculata, whereas species
commonly stimulated by fresh organic material (N. iridea, C. laevigata)
nearly disappeared. In the years to come, one of our main challenges
for improving the applicability of benthic foraminifera in both recent
environmental monitoring and in palaeoecological interpretations
studies will be to get a more detailed understanding of their trophic
strategies.
5. Conclusions
Bathyal (320 m) surface sediments and associated bottom water
from the Skagerrak (North Sea) were maintained in closed containers,
under dark, ambient temperature conditions for two years (2002 to
2004). No food or nutrients were added. In order to study their
response to a halt in the supply of freshly produced phytodetritus, the
living (stained) benthic foraminiferal content was examined before
and after the two year period. Because no fresh organic material from
primary production was available, the foraminifera were left to feed
on the organic material present in the sediment at the time of
collection, the associated bacteria, and on degradation products. In the
original assemblage, the abundance of allogromiids relative to other
taxa was comparable to that of the deep sea. Based on changes in
relative abundance three species response-categories are defined.
Category 1 includes taxa (allogromiids, Nonionella iridea, Cassidulina
laevigata), which probably depend on seasonal supply of fresh
phytodetritus to maintain their populations and therefore, nearly
disappeared. Category 2 includes taxa (e.g., Leptohalysis gracilis,
Melonis barleeanum, Adercotryma wrighti, Haplophragmoides bradyi)
which increased their abundance from rare (b0.5%) to common (2–
9%). They probably have a feeding strategy which is not dependent on
regular supply of fresh organic material but utilize refractory organic
material and degradation products. Category 3 includes taxa (e.g.,
Textularia earlandi, Globobulimina auriculata, Liebusella goësi, Stain-
73
forthia fusiformis, Eggerelloides medius) that are able to maintain their
populations for two years without supply of fresh organic material.
They are probably able to decrease their metabolism for a couple of
years and, in the same way as the category 2-species, they seem to
have a varied diet. Overall, the relative abundance of agglutinated
forms increased at the expense of allogromiids and calcareous forms
but the faunal response was not dramatic, as six of the seven most
abundant species in the 2002 and 2004 assemblages were the same.
The similarity in faunal composition between the two data sets was
56% for the smaller (63–125 μm) size fraction and 85% for the larger
(N125 μm) fraction showing that the main change occurred among
the smaller taxa. Still, the reduction in species diversity was moderate.
The results demonstrate that some foraminiferal species have a
particular resilience and survival potential to withstand extended
periods (here 2 years) without a supply of fresh organic material. In
other words, assemblages already adapted to an environment
dominated by supply of refractory, organic material stand a better
chance to survive periods when oceanic primary production is
reduced or ceases for a while, e.g., in response to extraterrestrial
impacts. The present experimental approach (but with better control
of environmental parameters) may prove useful to test trophic
strategies in other foraminiferal taxa.
Acknowledgements
Without Bruce Corliss' kind gesture to deviate from the original
schedule and stop the RV Arne Tisselius in the middle of the Skagerrak
to allow sampling to take place, this paper would never have been
written. I am also grateful to Lennart Bornmalm for logistical help
with the research cruise and to John W. Murray, Bruce Corliss, and an
anonymous reviewer for helpful suggestions and comments on the
manuscript. The research cruise was supported by NSF Grant OCE0133010.
Appendix A. Faunal reference list
Generic classification follows Loeblich and Tappan (1987). The
original descriptions can be found in the Ellis and Messina world
catalogue of foraminiferal species on http://www.micropress.org. The
taxa are listed alphabetically.
Adercotryma wrighti Brönnimann and Whittaker, 1987.
Bolivinellina pseudopunctata (Höglund) = Bolivina pseudopunctata
Höglund, 1947.
Cassidulina laevigata d'Orbigny, 1826.
Eggerella europeum (Christiansen) = Verneuilina europeum Christiansen,
1958.
Eggerelloides medius (Höglund) = Verneuilina media Höglund, 1947.
This is not a commonly reported species, probably misidentified as
Eggerelloides scaber.
Epistominella vitrea Parker, 1953.
Globobulimina auriculata (Bailey) = Bulimina auriculata Bailey, 1851.
In the present study, due to high degree of morphological
similarity (particularly in smaller individuals), this form also
comprises G. turgida (Bailey). The former has priority as it was
described prior to the latter.
Haplophragmoides bradyi (Robertson) = Trochammina bradyi Robertson,
1891.
Hippocrepinella alba Heron-Allen and Earland, 1932.
Leptohalysis gracilis (Kiaer) = Nodulina gracilis Kiaer, 1900 (part.).
Liebusella goësi Höglund, 1947. Probably the same as Martinottiella sp.1
in deStigter et al. (1998), as Bigenerina cylindrica in Koho et al.
(2008), and as Clavulina cylindrica in Hess and Jorissen (2009).
Melonis barleeanum (Williamson) = Nonionina barleeana Williamson,
1858.
Micrometula hyalostriata Nyholm, 1952.
Nonionella iridea Heron-Allen and Earland, 1932.
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Pullenia osloensis Feyling-Hanssen, 1954.
Reophax fusiformis (Williamson) = Proteonina fusiformis Williamson,
1858.
Stainforthia fusiformis (Williamson) = Bulimina pupoides d'Orbigny
var. fusiformis Williamson, 1858.
Textularia earlandi Parker, 1952 = Textularia tenuissima Earland, 1933.
For comments, see Alve and Goldstein (2010).
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