Progress in Oceanography 50 (2001) 261–283
www.elsevier.com/locate/pocean
Morphological and ecological parallels between sublittoral
and abyssal foraminiferal species in the NE Atlantic: a
comparison of Stainforthia fusiformis and Stainforthia sp.
Andrew J. Gooday
a
a,*
, Elisabeth Alve
b
Southampton Oceanography Centre, Empress Dock, European Way, Southampton SO14 3ZH, UK
b
Department of Geology, University of Oslo, Box 1047 Blindern, N-0316 Oslo, Norway
Abstract
Dead specimens of a minute fusiform rotaliid foraminifer are common in the 28–63 µm fraction of multiple corer
samples from a 4850 m-deep site on the Porcupine Abyssal Plain (PAP). Their test morphology is remarkably similar
to small specimens of Stainforthia fusiformis (Williamson, 1858), a species which is well known from coastal settings
(intertidal to outer shelf) around NW Europe and North America. A detailed comparison of the PAP form with typical
individuals of S. fusiformis from Norwegian waters (55–203 m depth), however, reveals slight but consistent morphological differences. The PAP specimens are smaller (test length 40–140 µm) than those from Norway (test length 80–
380 µm), the chambers tend to be rather less elongate, the density of pores in the test wall is much lower, and there
are differences in apertural features. We therefore conclude that the diminutive abyssal form is a distinct species, here
referred to as Stainforthia sp. This interpretation is consistent with increasing evidence for genetic differentiation in
deep-sea organisms, particularly along bathymetric gradients. Stainforthia sp. was previously illustrated by Pawlowski
as Fursenkoina sp. and appears to be widespread and abundant in the abyssal North Atlantic (⬎4000 m depth). Stainforthia fusiformis, on the other hand, is most abundant in continental shelf and coastal settings. It extends onto the
continental slope in the North Atlantic but has not been reported reliably from depths greater than about 2500 m.
We suggest that the striking morphological convergence between these two species reflects the adoption of similar
ecological strategies in widely separated habitats. Both are enrichment opportunists, a life-style which may explain the
rather broad bathymetric range of Stainforthia fusiformis. This is a dominant species in organically-enriched and sometimes extremely oxygen-depleted environments on the continental shelf, and is a rapid coloniser of formerly azoic
habitats. Live specimens of the abyssal form are typically found embedded within phytodetrital aggregates (organic
material derived from primary production in the euphotic zone). It is presumably the availability of these organic-rich
microhabitats, which enables this species to survive in the otherwise oligotrophic deep sea.  2001 Published by
Elsevier Science Ltd.
* Corresponding author. Fax: +44-23-8059-6353.
E-mail address: ang@soc.soton.ac.uk (A.J. Gooday).
0079-6611/01/$ - see front matter  2001 Published by Elsevier Science Ltd.
PII: S 0 0 7 9 - 6 6 1 1 ( 0 1 ) 0 0 0 5 7 - X
262
A.J. Gooday, E. Alve / Progress in Oceanography 50 (2001) 261–283
Contents
1.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 262
2.
Materials and methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 263
3. Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.1. Description of Stainforthia sp. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.1.1. Microspheric form . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.1.2. Megalospheric form . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.2. Occurrence of Stainforthia sp. at the PAP: size fractions and microhabitats . . . . . . . . . . . . . .
3.3. Comparison of Stainforthia sp. with Stainforthia fusiformis from the Oslofjord and Lyngdalsfjord
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
264
264
264
268
268
269
4. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.1. Taxonomic status of the shallow- and deep-water forms . . . . . . . . . . . .
4.2. Environmental influences on test morphology? . . . . . . . . . . . . . . . . .
4.3. Bathymetric ranges . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.4. Parallel ecological strategies among shallow and deep-water foraminifera?
4.5. Significance of micro- and megalospheric forms . . . . . . . . . . . . . . . .
4.6. Geological implication . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
273
273
274
274
277
277
278
5.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
Concluding remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 278
6. Taxonomic notes . . . . . . . . . . . . .
6.1. Stainforthia fusiformis (Williamson)
6.1.1. Generic placement . . . . . . . . .
6.1.2. Apertural features . . . . . . . . .
6.1.3. Williamson’s syntypes . . . . . .
6.1.4. Material of Millett . . . . . . . .
6.2. Stainforthia sp. . . . . . . . . . . . .
6.2.1. Generic placement . . . . . . . . .
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
279
279
279
279
280
280
280
280
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 280
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 281
1. Introduction
The seasonal deposition of phytodetritus following the spring bloom is well documented in the temperate
North Atlantic, a region where the bloom is stronger and more extensively developed than in any other
oceanic area (Longhurst, 1998). The benthic response to these food inputs is most evident among the
smaller organisms, particularly bacteria and protists (Pfannkuche 1992, 1993; Lochte, 1992), although there
is evidence that it also triggers seasonal reproduction and growth in a number of larger metazoans (Lampitt,
1990; Campos-Creasey, Tyler, Gage, & John, 1994). The foraminifera, which make a major contribution
to deep-sea benthic communities (Tendal & Hessler, 1977; Snider, Burnett, & Hessler, 1984; Gooday,
Levin, Linke, & Heeger, 1992), are one of the taxa that clearly respond to phytodetrital pulses. Time-series
studies suggest that opportunistic foraminiferal species undergo rapid reproduction and population growth
following phytodetrital inputs to the ocean floor (Gooday & Lambshead, 1989; Gooday, & Turley, 1990;
Gooday, 1993).
A.J. Gooday, E. Alve / Progress in Oceanography 50 (2001) 261–283
263
In the abyssal NE Atlantic, foraminiferal responses to phytodetrital inputs have been reported at two
sites, the BIOTRANS area (Gooday, 1988) and the Porcupine Abyssal Plain (PAP) (Gooday 1993, 1996).
Many of the species involved are small calcareous forms with thin-walled transparent tests. They include
Epistominella exigua and Alabaminella weddellensis, both well-known species that are concentrated in the
63–125 µm size fraction of sediment samples. Also present at the BIOTRANS and PAP sites is a minute
fusiform species. Living individuals of this form are confined to the phytodetritus whereas the dead tests
are almost entirely restricted to sediment residues finer than 63 µm, a size fraction examined rarely in
foraminiferal studies (Pawlowski & Lapierre, 1988; Pawlowski, 1991; Pawlowski, Lee, & Gooday, 1993;
Gooday, Carstens, & Thiel, 1995). These tiny foraminifera closely resemble small individuals of Stainforthia fusiformis (Williamson), a species which is known mainly from the continental shelf of NW Europe
and North America (Alve, 1994). At first sight, the similarity seemed so close that we were tempted to
refer them to the same species. However, a careful examination of the test morphology suggests that they
are not conspecific. In this paper, we compare specimens from the PAP site to S. fusiformis from shallowwater sites in Norwegian fjords, and discuss the taxonomic and ecological implications of the close morphological similarities between them.
2. Materials and methods
Sampling localities are listed in Table 1. At the PAP, samples were collected using a multiple corer
(Barnett, Watson, & Connelly, 1984). Any phytodetritus present on the core surface was first removed using
a pipette or forceps and then preserved in 4% formalin buffered with sodium borate (borax). Individual cores
(25.5 cm2 surface area) obtained during RRS Discovery Cruise 185 were subsampled to a depth of ⬎5
cm using a 20 ml syringe with the end cut off to create a small piston corer. These subcores were extruded,
sliced into 1 cm-thick sections down to 5 cm depth, and each slice was fixed in buffered formalin. In the
case of samples from deployments 11908#33, 39, 70, the entire core was cut into 1 cm-thick slices. Multiple
corer samples obtained during RV Meteor Cruise 42/2 were sliced into 1 cm-thick layers down to 10 cm
depth and fixed in buffered formalin. Samples from the Oslofjord and Lyngdalsfjord (both in southern
Norway) were collected using a gravity corer. The sediment cores (69-mm diameter) were sectioned into
Table 1
Sampling locations
Cruise or locality
Station and gear
deployment number
Porcupine Abyssal Plain samples
Discovery 185
11908#03
Discovery 185
11908#05
Discovery 185
11908#06
Discovery 185
11908#16
Discovery 185
11908#33
Discovery 185
11908#39
Discovery 185
11908#70
Meteor 42/2
421#02
Norwegian samples
Oslofjord
C1-K2
Lyngdalsfjord
YL5
Position
Depth (m)
Latitude
Longitude
48°
48°
48°
48°
48°
48°
48°
48°
16°
16°
16°
16°
16°
16°
16°
16°
55.2⬘N
51.2⬘N
51.0⬘N
51.9⬘N
49.7⬘N
49.9⬘N
49.5⬘N
58.05⬘N
59° 39.07⬘N
58° 09.98⬘N
29.7⬘W
29.9⬘W
27.0⬘W
29.3⬘W
27.3⬘W
30.1⬘W
30.4⬘W
28.1⬘W
10° 36.59⬘E
06° 49.53⬘E
4847
4843
4851
4847
4847
4845
4847
4881
55
203
264
A.J. Gooday, E. Alve / Progress in Oceanography 50 (2001) 261–283
1 cm slices and preserved in ethanol. Only the upper (0–1 cm) sediment layers have been examined for
this study.
In the laboratory, the sediment was either washed on 63 µm and 28 µm sieves to isolate the finest
fraction, or washed directly on a 28 µm sieve (⬎28 µm fraction). In the case of the Norwegian material,
the finest sieve used was 32 µm. The sieve residues were placed in a glass Petrie dish and examined in
water under a binocular microscope. Specimens of Stainforthia fusiformis were removed using a fine pipette
and either stored dry on micropalaeontological slides or placed directly into glycerol in a glass cavity slide.
For light photomicroscopy, specimens were remounted in glycerol on a flat glass slide, covered with a
coverslip supported by fine glass beads, and photographed using an Olympus compound photomicroscope.
Line drawing of specimens mounted in the same way were drawn using a drawing tube attached to a Wild
M5 compound microscope. For scanning electron microscopy (SEM), dried specimens were mounted on
stubs using double-sided tape, coated in gold and examined in a Jeol JSM 840 SEM.
3. Results
3.1. Description of Stainforthia sp.
3.1.1. Microspheric form
The vast majority of individuals from the PAP site are microspheric (i.e. they belong to the diploid,
gamont generation, which reproduces asexually). The tests range in length from 40 to 150 µm and in width
from 30 to 80 µm (Table 2 and Figs. 1 and 2). Each test is elongate, approximately fusiform in shape, is
widest anterior to the mid-point tapering towards both the rounded apertural and proximal ends, and is
slightly flattened to give an ovate cross-section [Fig. 3(K–Y); Pl. 1, Figs. A–G]. The length:width ratio
varies from 1.5 to 3.3 with a strong aggregation of values around 2.0. Twenty-six randomly selected
specimens from RV Meteor station 421#2 have 5–11 (mean 8.3±1.5) twisted, biserially-arranged chambers,
which increase in size and become progressively more elongate distally. The proloculus of these specimens
is spherical and 12–21 µm in diameter (Fig. 4). The chambers are somewhat inflated and overlap each
other to a considerable extent, particularly in the earlier stages [Fig. 3(K–Y)]. The sutures are clearly
developed and somewhat depressed.
Table 2
Test dimensions of Stainforthia sp. (PAP) and Stainforthia fusiformis (Norwegian sites). ND=no data
Locality and size fraction
Stainforthia sp.
PAP: 28–63 µm
PAP: ⬎28 µm
PAP: all specimens
Stainforthia fusiformis
Oslofjord: ⬎63 µm
Lyngdalsfjord: ⬎32 µm
Length
Width
Length:width
range: 40–140 µm mean
84.4±21.0 µm, n=315
range: 50–150 µm mean:
92.2±22.2 µm n=222
range: 40–150 µm mean:
87.6±22.2 µm n=537
range: 30–60 µm mean:
48.6±7.3 µm n=50
range: 30–80 µm mean:
45.8±9.7 µm n=222
range: 30–80 µm mean:
46.3±9.3 µm n=272
range: 1.5–2.67 mean:
2.10±0.26 n=50
range: 1.5–3.33 mean:
2.01±0.26 n=222
range: 1.5–3.33 mean:
2.02±0.26 n=272
Range: 120–320 µm mean:
190.8±32.3 µm n=453
Range: 80 to 380 µm mean:
178.3±57.9 µm n=272
ND
ND
ND
ND
A.J. Gooday, E. Alve / Progress in Oceanography 50 (2001) 261–283
265
Fig. 1. Distribution of test lengths for specimens of Stainforthia fusiformis from the Oslofjord and Lyngdalsfjord (Norway) and of
Stainforthia sp. from the Porcupine Abyssal Plain. In the lower panel, the bars represent cumulative totals of specimens from the
28–63 µm and ⬎28 µm size fractions.
Fig. 2. Stainforthia sp. from the Porcupine Abyssal Plain: test length vs width. Microspheric individuals indicated by circles, megalospheric individuals by diamonds. The numbers indicate the number of specimens.
266
A.J. Gooday, E. Alve / Progress in Oceanography 50 (2001) 261–283
Fig. 3. Optical sections of tests mounted in glycerol. A–J, specimens of Stainforthia fusiformis from Lyngdalsfjord (Norway); K–
Y, specimens of Stainforthia sp. from the Porcupine Abyssal Plain. Scale bar=100 µm.
The aperture is situated at the base of the final chamber and lies within a depressed area that occupies
most of the face of this chamber (Plate 2). It is bordered on one side by an elongate toothplate, which
typically is fairly straight, at least when the test is viewed in its natural resting position (Pl. 2, Figs A–
C). In some individuals the toothplate is more curved; in one example, it forms a semi-circular loop
around the aperture (Pl. 2, Fig. F). The toothplate usually has a straight edge but occasionally is very
weakly serrated.
The test wall is very thin, delicate and transparent with a smooth, shiny surface. Examination under a
A.J. Gooday, E. Alve / Progress in Oceanography 50 (2001) 261–283
267
Plate 1. Transmitted light micrographs of specimens mounted in glycerol. Figs. A–G. Stainforthia sp. from the Porcupine Abyssal
Plain (Discovery Station 11908); Fig. D is megalospheric, the others are microspheric. Figs. H–L. Stainforthia fusiformis from Lyngdalsfjord, Norway. Test lengths are as follows: 136 µm (A), 109 µm (B), 123 µm (C), 143 µm (D), 62 µm (E), 65 µm (F), 103 µm
(G), 151 µm (H), 105 µm (I), 145 µm (J), 145 µm (K), 118 µm (L).
polarising microscope reveals that it has a radial structure. The wall is perforated by occasional tiny,
scattered pores, 270–450 nm diameter (Pl. 2, Fig. J).
268
A.J. Gooday, E. Alve / Progress in Oceanography 50 (2001) 261–283
Fig. 4. Proloculus diameters for specimens of Stainforthia fusiformis from the Oslofjord and Lyngdalsfjord (Norway) and of Stainforthia sp. from the Porcupine Abyssal Plain. The bars show cumulative totals.
3.1.2. Megalospheric form
Five dead individuals (Fig. 5), 3 from the 63–125 µm fraction (RV Meteor station 421#2) and 2 from
the 28–63 µm fraction (RRS Discovery station 11908#05), may represent the megalospheric generation
(i.e. the diploid, agamont generation which reproduces sexually). The two specimens from sample 11908#05
were among 222 individuals picked at random from the ⬎28 µm fraction, an incidence of ⬍1%. These
five specimens are larger than most microspheric individuals. Length: 140, 175, 184, 205 and 235 µm;
width: 76, 86, 77, 82, 100 µm; length/width ratio: 1.84, 2.03, 2.35, 2.49, 2.35; proloculus diameter: 31,
35, 31, 33.5, 28.9 µm (Fig. 4). The number of chambers ranges from 6 to 9. The aperture is situated fairly
close to the end of the test and the apertural depression is developed only weakly. The toothplate is
prominent and linear. In one specimen examined by SEM, the toothplate clearly curves around the aperture
at its distal end, as in some of the microspheric specimens.
3.2. Occurrence of Stainforthia sp. at the PAP: size fractions and microhabitats
At the PAP site, dead individuals of Stainforthia sp. were more or less restricted to the 28–63 µm
fraction. In three of the samples, it contributed up to 16, 21 and 29% of all the dead tests in this size
range, whereas only very occasional specimens were encountered in the ⬎63–125 µm fraction (Table 3).
‘Live’ (rose Bengal stained) specimens were uncommon and mainly occurred within phytodetritus aggregates where they contributed up to about 10% of the entire live phytodetrital assemblage. These individuals
contained green protoplasm and presumably had ingested algal cells derived from the aggregates. A few
live specimens were also found in the upper 1 cm layer of sediments overlain by phytodetritus; these too
contained green protoplasm and had probably originated from the phytodetrital layer.
A.J. Gooday, E. Alve / Progress in Oceanography 50 (2001) 261–283
269
Plate 2. Stainforthia sp.: scanning electron micrographs of specimens from the Porcupine Abyssal Plain. Figs. A, B, D, E, entire
tests in their natural resting positions. Figs. F, G, tests which have been tilted to obtain clearer view of aperture. Figs. C, H, I,
apertural details. Fig. J detail of wall with scattered pores. Scale bars: 50 µm (D,G). 40 µm (A,B), 20 µm (E,F), 10 µm (C,H–J).
3.3. Comparison of Stainforthia sp. with Stainforthia fusiformis from the Oslofjord and Lyngdalsfjord
Stainforthia fusiformis is a common, widely distributed species on the continental shelf and upper slope
around NW Europe and North America including the Canadian Arctic (Murray, 1991). It is an abundant
and sometimes dominant component of living assemblages in the North Sea and Norwegian fjords (Murray,
270
A.J. Gooday, E. Alve / Progress in Oceanography 50 (2001) 261–283
Fig. 5. Stainforthia sp.: megalospheric individuals from the Porcupine Abyssal Plain; optical sections of tests mounted in glycerol.
A,B,D, RV Meteor station 421#2, ⬎63 µm fraction; C, E, RRS Discovery Station 11908#5, 28–63 µm fraction. Scale bar=100 µm.
Table 3
Occurrence of dead and live specimens of Stainforthia sp. in PAP samples. The dead specimens were derived from the 0–1 cm
sediment layer, the live specimens from the 0–1 cm sediment layer and the phytodetritus. Three of the 4 dead specimens from Sample
421#2 were megalospheric individuals. Percentages in parentheses indicate proportion of assemblage
Station and deployment
number
11908#06
11908#16, core 7
11908#16, core 8
11908#26
11908#33 core 7
11908#33 core 2
11908#39
11908#70
421#2
Number dead,
28–63 mm
ND
153 (21.2%)
ND
ND
134 (28.7%)
ND
ND
ND
21 (15.8%)
Number: dead,
⬎63 mm
ND
1
ND
ND
0
ND
ND
ND
4
Live
In phytodetritus
0–1 cm layer
5 (9.8%)
6 (3.1%)
5 (4.1%)
2 (6.2%)
6 (7.6%)
11 (7.6%)
4 (2.0%)
2 (7.1%)
ND
ND
2 (1.1%)
1 (1.0%)
ND
2 (1.3%)
2 (0.4%)
0
0
ND
1992; Alve, 1995). Live individuals also occur occasionally at an intertidal site in southern England (Alve &
Murray, 2001). Alve and Murray (unpublished data) found specimens from the Norwegian waters to be
virtually identical to the type specimens in the Natural History Museum, London (see taxonomic notes).
We therefore made a detailed comparison of the PAP form and typical Norwegian specimens of S.
A.J. Gooday, E. Alve / Progress in Oceanography 50 (2001) 261–283
271
fusiformis using light and scanning electron microscopy. The general appearance of the test and the shape
and arrangement of the chambers is remarkably similar in the two forms, particularly when they are viewed
as optical sections (Fig. 3 and Pl. 1). However, a close examination reveals some differences (Table 4).
1. Specimens of S. fusiformis are typically larger than the PAP forms. Four hundred and fifty three specimens from the Oslofjord (55 m water depth) measured 120–320 µm (mean 191±32 µm) long (Table 2
and Fig. 1). Höglund (1947, Figure 232 therein) reported a similar size range (130–340 µm) for specimens from the Gullmarfjord (his Stn G11, 44 m depth) on the Swedish west coast. Measurements of
the Oslofjord specimens were based on the 63 µm sieve fraction in which very small specimens were
not represented. We therefore measured an additional 272 specimens from the ⬎32 µm fraction of a
sample collected in Lyngdalsfjord (203 m depth); this was comparable to the ⬎28 µm sieve fraction
used for the PAP samples. These individuals varied from 80 to 380 µm in length (mean 178±58 µm).
In contrast, the PAP form is (with the exception of a few megalospheric individuals) between 40 and
150 µm long (Table 2).
2. The chambers in Stainforthia fusiformis tend to be relatively elongate and there is a greater degree of
overlap between adjacent chambers, which are separated by fairly steeply-angled sutures. In the PAP
form, the chambers are shorter, do not overlap so extensively, and the sutures that separate them are
less steeply inclined (e.g. compare Pl. 2, Figs. A, B and Pl. 3, Figs. A, B). This distinction is much
less clear in the smaller individuals (e.g. compare Pl. 1, Figs. F and L; test lengths 65 and 118 µm
respectively). The small proximal chambers in S. fusiformis often project as a short, blunt ‘tail’ beneath
the larger later chambers (Pl. 1, Figs. J, K; Pl. 3, Fig. A; see also Höglund, 1947, Figs. 227, 228 therein).
This feature is, at most, developed only weakly in the abyssal form.
3. Pores in the test wall are larger and much more densely developed in Stainforthia fusiformis than in
the abyssal form (compare Pl. 2, Fig. J and Pl. 3, Fig. J).
4. There are differences in the apertural region, which are particularly evident when the tests are in a stable
resting position with the aperture facing obliquely upwards. In Stainforthia fusiformis, the aperture is
usually clearly defined and lies well away from the end of the chamber in a prominent spoon-shaped
depression which becomes narrower and shallower distally (Pl. 3, Figs. A–C, G, H; Höglund, 1947,
Figs. 219–222 therein). A prominent, strongly serrated apertural lip arises from the face of the final
Table 4
Summary of differences between Stainforthia sp. (Porcupine Abyssal Plain) and Stainforthia fusiformis (Norwegian waters)
Test feature
Stainforthia sp.
Stainforthia fusiformis
Size
Test morphology
40–150 µm
(i) Chambers rather elongate, strongly
overlapping; sutures steeply angled.
(ii) Tendency for chambers to increase
evenly in size, leading to rather smoothly
fusiform shape
Pores
Aperture and associated features
Smaller (270–450 nm), sparse
(i) Aperture closer to end of test, spoonshaped depression not well developed
80–380 µm
(i) Chambers relatively shorter, overlap
less.
(ii) Tendency for later chamber to increase
more rapidly in size, leading to bulbous
(distal) and narrower (proximal) regions of
test.
Larger (390–550 nm), dense
(i) Aperture located further away from end
of test; spoon-like depression usually well
developed
(ii) Apertural lip strongly serrated, curved
around aperture
(iii) Aperture often terminal in larger
individuals
(ii) Apertural lip non-serrated, appears
linear
(iii) Aperture never clearly terminal
272
A.J. Gooday, E. Alve / Progress in Oceanography 50 (2001) 261–283
Plate 3. Stainforthia fusiformis: scanning electron micrographs of specimens from the Oslofjord (A, B, D, G–I) and Lyngdalsfjord
(C, E, F, J), Norway. Figs. A–E, tests in their natural resting position (note the terminal aperture in D). Fig. F detail of specimen in
Fig. E, tilted to obtain clearer view of aperture. Note that this specimen is damaged and the view is of an inner chamber; the tube
(also visible in Fig. E) is part of the toothplate structure (see Höglund, 1947, Fig. 231; Pl. 20, Fig. 3 therein). Figs. G–I details of
aperture. Fig. J detail of wall with numerous pores. Scale bars: 100 µm (A–D), 50 µm (E, G/H), 20 µm (F), 10 µm (I, J).
A.J. Gooday, E. Alve / Progress in Oceanography 50 (2001) 261–283
273
chamber and forms a curved border encircling at least half of the aperture (Pl. 3, Fig. I; Höglund, 1947,
Pl. 20, Fig. 3 therein). A few specimens of S. fusiformis [14% of 418 stained individuals (⬎63 µm
fraction) from the Oslofjord site] have terminal apertures (Pl. 3, Fig. D) of the kind illustrated by Murray
(1971) and developed in many of Williamson’s syntypes (see below). In the PAP form, the face of the
final chamber is usually relatively shorter so that the aperture (located at the base of this chamber) lies
closer to the end of the test. As a result, the depression around the aperture is shorter and less obvious
than in S. fusiformis. The apertural lip is, at most, only very weakly serrated and usually forms a more
or less linear feature, at least when the test is in a stable resting position (clearly shown in Pl. 1, Fig.
5b of Pawlowski, 1991). These apertural differences are not clear cut, however, and there is some degree
of overlap. (i) In a few PAP specimens, the lip is curved and, in at least one case, forms a complete
(albeit non-serrate) border around the aperture, as in S. fusiformis. This feature is most evident when
specimen are orientated obliquely in order to obtain a direct view of the aperture (Pl. 2, Fig. F). (ii)
Although the PAP form never develops a true terminal aperture, the aperture is subterminal in a few
individuals (Pl. 2, Fig. G). In these cases, the shape and position of the ‘toothplate’ are similar to that
observed in the terminal aperture of S. fusiformis. (iii) A few Norwegian specimens of S. fusiformis
have a linear toothplate, similar to that of the PAP form (Pl. 3, Figs. E, F; however, note the comments
in the plate caption). (iv) The apertural depression is fairly prominent in some small PAP individuals
and approaches the spoon-shaped condition observed in S. fusiformis (Pl. 2, Fig. F).
4. Discussion
4.1. Taxonomic status of the shallow- and deep-water forms
Despite the remarkable similarity in the appearance of the test, particularly in small individuals, the
minor but consistent differences between Stainforthia and Stainforthia fusiformis strongly suggest that they
are distinct species. The density of test-wall pores and the position and morphology of the aperture seem
to be important distinguishing features.
Pore densities can be influenced by environmental factors; for example, they decrease with increasing
oxygen concentrations (Gary, Healy-Williams, & Ehrlich, 1989; Gary, 1991; Kitazato & Tsuchiya, 1999),
but not to an extent that would explain the differences observed in this study. The fact that high pore
densities occurred in populations of S. fusiformis from both the Lyngsdalsfjord (O2=0.28 ml/l just above
the sediment surface) and well-oxygenated environments in the Oslofjord and the open Skagerrak (North
Sea) (Olsgard, pers. comm.; Alve unpublished data), also suggests that the pore densities in our two species
are genetically rather than environmentally controlled. The diminutive size of the abyssal form has less
taxonomic significance. Dwarfism in foraminifera can arise when optimal conditions lead to rapid growth
and reproduction or, conversely, when the organisms are adversely affected by environmental stress
(reviewed by Boltovsky & Wright, 1976, pp. 90–92 therein; see also Murray, 1963; Pflum & Frerichs,
1976). It could be argued that the small size of the abyssal form reflects an impoverished food supply in the
oligotrophic deep sea, compared to the eutrophic conditions experienced by S. fusiformis in shelf settings.
Our interpretation of the abyssal and sublittoral forms as distinct species is consistent with evidence
that deep-sea organisms possess pressure- and temperature-sensitive biochemical systems (enzymes, cell
membranes, structural proteins) that define their upper and lower bathymetric limits (Somero, Siebenaller, &
Hochachka, 1982; Somero, 1991, 1992). In other taxa, opportunistic species often have broad bathymetric
ranges, but with upper limits that are temperature dependent. For example, the holothurian Kolga hyalina
ranges from 5000 m to 1500 m depth in the North Atlantic where its upper limit is apparently defined by
the 4°C isotherm (Billett, 1991). Increasing evidence for genetic differentiation and cryptic speciation in
274
A.J. Gooday, E. Alve / Progress in Oceanography 50 (2001) 261–283
the deep sea (e.g. Creasey & Rogers, 1999; Etter, Rex, Chase, & Quattro, 1999), also supports our view
that the two forms are distinct. An instructive example of cryptic speciation is provided by the lysianassid
amphipod Eurythenes gryllus, a cosmopolitan scavenger with a bathymetric range from 184 m to 6500 m.
In a study of the molecular genetics of E. gryllus, France and Kocher (1996) concluded that abyssal
populations from the central North Pacific, the NW and NE Atlantic, and the Arctic Oceans represent a
single, widely-distributed species. There was considerable genetic divergence, however, between abyssal
(⬎3500 m water depth) populations and non-abyssal (⬍3200 m depth) populations which consisted of a
number of cryptic species isolated by physical conditions within the bathyal zone. There were some corresponding minor morphological differences; for example, abyssal individuals were about 36% smaller, on
average, than those from bathyal depths.
4.2. Environmental influences on test morphology?
Of course, the striking environmental contrasts that exist between abyssal and shelf habitats may account
for some of the morphological differences between the two species. Both the quantity and quality of
available food are much lower in the oligotrophic deep sea than in fjords and other coastal areas. As
mentioned above, this may explain the smaller size of the PAP form. Specimens from the PAP also have
a larger number of chambers than Norwegian individuals of a similar size. This is clearly seen in the
specimens illustrated in Fig. 3 and suggests that the PAP form grows more slowly. Carbonate dissolution
may be a significant environmental factor at the PAP site. Murray (1963) suggested that a shortage of
calcium might result in smaller test sizes in estuarine foraminifera. The carbonate lysocline and compensation depth in this part of the Atlantic are around 4900 m and 5200 m respectively (Biscaye, Kolla, &
Turekian, 1976).
In shallow-water habitats, Stainforthia fusiformis is one of a number of foraminiferal species known to
sequester chloroplasts. Bernhard and Bowser (1999) suggest that the double-folded lip (terminal aperture)
or serrated toothplate (non-terminal aperture) of adult individuals may be used to hold diatoms so that the
frustules can be prised apart and the chloroplasts extracted. Sequestration of chloroplasts is highly unlikely
to occur in an abyssal foraminifer, and this may explain the lack of a clearly serrated toothplate in Stainforthia sp..
4.3. Bathymetric ranges
Specimens from the NW Rockall Bank (57° 05.31⬘N, 12° 24.25⬘W; 1920 m water depth) and 2200 m
depth to the south of Iceland (Pl. 4, Fig. A; Austin & Evans, 2000, Fig. 6.11 therein) indicate that Stainforthia fusiformis penetrates to bathyal depths in the NE Atlantic. These deep-water specimens are morphologically identical to those occurring in shallow water. Individuals from the Iceland Basin have a terminal
aperture and both interio-marginal and terminal apertures are present in the Rockall Bank material. Although
cryptic speciation has been reported among both planktonic and benthic foraminifera (Pawlowski, Bolivar,
Farhni, & Zaninetti, 1995; Darling, Kroon, Wade, & Leigh, 1996; Huber, Bijma, & Darling, 1997; De
Vargas, Norris, Zaninetti, Gibb, & Pawlowski, 1999), there is no morphological basis for regarding the
coastal and bathyal forms of S. fusiformis as distinct species. A genetic study at the molecular level,
however, is required to confirm this conclusion.
Other deep-water records (maximum water depth 4217 m) of Stainforthia fusiformis are more problematic
and usually the lack of any illustration means that the validity of these identifications cannot be evaluated.
Lagoe (1977) and Scott and Vilks (1991) report this species from ⬎3600 m in the Arctic Ocean (Table
5). The specimen illustrated by Lagoe (1977) is convincing, but it is not clear from the figure caption
whether it originated from a deeper (3678–3809 m) or a shallower (1363–1855 m) site. The figured specimens of Scott and Vilks (1991) from the Arctic Ocean and Hermelin and Scott (1985) from the central
A.J. Gooday, E. Alve / Progress in Oceanography 50 (2001) 261–283
275
Plate 4. Stainforthia fusiformis. A. Specimen from 2200 m depth in the Iceland Basin; note the terminal aperture (specimen courtesy
of Dr. W.E.N. Austin). B. Brocken specimen from Oslofjord station C1–K2 (surface 1 cm) with terminal aperture and juvenile interiomarginal aperture.
North Pacific are probably not S. fusiformis. Test measurements derived from the illustration of Echols
(1971) and Wollenburg and Mackensen (1998b) indicate that the bathyal individuals (from 1032 m and
562 m water depth respectively) they assign to S. fusiformis fall within the size range (130–300 µm) of
shallow-water specimens (Table 5). We therefore conclude that in the Arctic and North Atlantic Oceans,
this species ranges from intertidal habitats to the bathyal zone; i.e. down to at least 2200 m and possibly
to 苲3000 m if the deeper records of Echols (1971) and Wollenburg and Mackensen (1998b) are accepted
(Table 5).
Pawlowski and Lapierre (1988) and Pawlowski (1991) discovered a tiny form (⬍120 µm long) which
is identical to our Stainforthia sp., in the 32–63 µm fraction of samples from abyssal sites in the NE
Atlantic and on the Bermuda Rise (NW Atlantic). They identified it as Fursenkoina sp. Pawlowski (1991)
commented that his specimens were “possibly a deep water form of the highly variable and widespread
group of F. fusiformis-schreibersiana.” At both sites, it made up a substantial proportion of the assemblage
in the finest (32–63 µm) residue. Living individuals of the same species were recognised later at ⬎4800
m depth at the PAP (Gooday et al., 1995; Gooday, 1996) and the nearby BIOTRANS site (Gooday, 1988;
as Bulimina sp.). Consequently, Stainforthia sp. appears to be widespread at abyssal depths (⬎4000 m) in
276
A.J. Gooday, E. Alve / Progress in Oceanography 50 (2001) 261–283
Table 5
Records of Stainforthia fusiformis from water depths exceeding 1000 m
Reference
Area
Depth
Test length
Method
Caralp, Lamy, and Pujos
(1970)
Echols (1971)
Bay of Biscay
850–3200 m
No size data
Southern Ocean;
off South Georgia
1032 m, 1500 m,
1900 m, 2924 m
287 µm, 283 µm
(from Pl. 12, Fig.
6, 7)
250 µm (from Pl.
4, Fig. 14)
Total assemblages
?size
Total assemblages
⬎62 µm, 125 µm
Hermelin and Scott (1985) Central North
Atlantic
540–2760 m
Lagoe (1977)
Central Arctic
Ocean
1363–1855 m or
3678–3809 m
Scott and Vilks (1991)
Arctic Ocean
1570 m, 1980 m,
3920 m, 4217 m
Wollenburg and
Mackensen (1998a,b);
Wollenburg (1992)
Yermak Plateau,
Arctic Ocean
1394 m, 2994 m
Bergsten (1994)
Yermak Plateau,
Arctic Ocean
Morris Jesup Rise,
Arctic Ocean
Wilmington and
South Heyes
Canyons, NE
Atlantic
Submarine canyons
off New Jersey
E. flank of
Reykjanes Ridge,
56–63°N, 22–28°W
2485 m
Bergsten (1994)
Lundquist, Culver, and
Standley (1997)
Swallow and Culver
(1999)
Austin and Evans (2000)
Lutze (1980)
Off Morocco
1083 m
1501–2503m
Comments
Figured specimens
(from 1032 m)
fairly typical
Total assemblages, Figured specimen
⬎63 µm
very slender;
probably not S.
fusiformis
240 µm (from Pl. Unstained ⬎62 µm Figured specimen
4, Fig 5)
residue
convincing but
depth of origin not
indicated
455 µ (from Pl. 2, Unstained ⬎63 µm Large specimen
Fig. 8)
with short terminal
spine; probably not
S. fusiformis
132–308 µm
⬍1% of live
Illustrated specimen
assemblages ⬎63 (from 562 m)
µm
slender but
otherwise
convincing
No size data
Dead assemblage ⬍0.3% of dead
⬎63 µm
assemblage
No size data
Dead assemblage 1.9–2.5% of dead
⬎63 µm
foraminifera
No size data
Total assemblages 1.6–24.6% of
⬎63 µm
assemblage
1473–2475m
No size data
1092–2820 m
187, 193 µm (our
measurements)
1854 m
No size data
Live assemblages,
⬎63 µm
Total assemblages
⬎63 µm
Live assemblage,
⬎63 µm
Up to 2% of live
assemblage
Specimens from
2221 m have
terminal apertures
(Pl. 4, Fig. B; Fig.
6.11 of Austin &
Evans, 2000)
‘Subspecies’ which
is “More slender
and elongate than
fusiformis, but
showing the typical
terminal aperture of
adult forms...”
the North Atlantic. The occurrence of live specimens at the PAP and BIOTRANS localities confirms that
Stainforthia sp. is indigenous to the abyssal NE Atlantic and not introduced either by currents (see Alve,
1999 for a review) or down-slope transport mechanisms, as reported for some other deep-water foraminiferal species (Groot, Benson, & Wehmiller, 1995).
A.J. Gooday, E. Alve / Progress in Oceanography 50 (2001) 261–283
277
4.4. Parallel ecological strategies among shallow and deep-water foraminifera?
Stainforthia fusiformis can survive in a variety of different food-input regimes and is by no means always
abundant. Where food is plentiful, however, its opportunistic characteristics become obvious (Alve, 1994).
This species shows rapid fluctuations in population size down core profiles and is an extremely successful
recoloniser of formerly anoxic environments (Alve, 1995) as well as new, recently established habitats
(Alve, 1999). It exploits food resources in organic-rich, oxygen-depleted muddy sediments and is inferred
to grow and reproduce quickly throughout the year and to have a high turnover rate (Murray, 1992). Live
specimens of Stainforthia sp. at the PAP site were also associated with organically-enriched microhabitats.
They always occurred either within aggregates of relatively fresh phytodetritus or, occasionally, in sediments directly beneath the phytodetrital deposits (Table 3), but were never encountered in samples devoid
of phytodetritus. Thus, S. fusiformis and Stainforthia sp. are both associated with high concentrations of
organic matter, either in the environment generally or in small localised microhabitats. Stainforthia apertura
exhibits a similar opportunistic life-style at bathyal depths in Sagami Bay, Japan (Ohga & Kitazato, 1997;
as Fursenkoina sp. 1). Given the right circumstances (i.e. a supply of labile food material), deep-water
foraminifera seem just as capable of ‘bloom-feeding’ as their shallow-water counterparts (Lee, Muller,
Stone, McEnery, & Zucker, 1969; Gooday, 1988). We conclude that similar ecological adaptations have
arisen among calcareous benthic foraminifera irrespective of bathymetric setting, leading to the evolution
of some remarkable morphological similarities between species living on continental shelves and abyssal
plains.
4.5. Significance of micro- and megalospheric forms
We document the rare (⬍1%) occurrence at the PAP site of individuals resembling Stainforthia sp. but
having a proloculus that is clearly larger than in typical specimens (Fig. 4). These can be interpreted in
several ways. They could be megalospheric gamonts, which are produced asexually but reproduce sexually.
Note that megalospheric forms have a bigger proloculus than microspheric forms, although this is not
always the case (see Lee, Faber, Anderson, & Pawlowski, 1991 for a review). This scenario, however,
makes it difficult to interpret the ‘normal’ forms with small proloculi. If these are agamonts, which are
produced sexually but reproduce asexually, then sexual reproduction must be widespread in Stainforthia
sp. Yet it seems highly unlikely that sexual reproduction by a few megalospheric gamonts could yield such
a large number of microspheric agamonts, which, in turn, produce just a few megalospheric gamonts
through asexual reproduction. Moreover, as Murray (1991) points out, sexual reproduction is probably
unusual for foraminiferal species living in the sparsely populated deep sea. Alternatively, ‘normal’ individuals of Stainforthia sp. could be schizonts which repeatedly reproduce asexually, although it is not clear
why they should have a significantly smaller proloculus than asexually-produced gamonts. Another possibility, which offers the simplest solution to this problem, is that the ‘megalo’- and ‘microspheric’ forms
at the PAP site are, in fact, different species.
Test dimorphism has not been recognised in Stainforthia fusiformis, despite an exhaustive study by
Höglund (1947) who measured the proloculus diameter of 740 specimens from two stations in the
Gullmarfjord. The range was 10–25 µm with a peak at 15 µm (Höglund, 1947, Fig. 233 therein). He
concluded that it was not possible, on the basis of his data, to distinguish between micro- and megalospheric
forms and was unable, therefore, to decide which generation his specimens represented. Höglund’s (1947)
proloculus data are remarkably similar to our more limited measurements of proloculus diameters in
microspheric individuals of Stainforthia sp. and in our Norwegian specimens of Stainforthia fusiformis.
The completely unimodal distribution of the proloculus size data in S. fusiformis (based on 758 specimen,
including those examined for this study) contrasts with the bimodal (albeit highly unbalanced) distribution
observed in Stainforthia sp. Thus, reproduction in S. fusiformis may be entirely asexual, as reported in
278
A.J. Gooday, E. Alve / Progress in Oceanography 50 (2001) 261–283
Fissurina marginata and Spiroloculina hyalina (Goldstein, 1999, p. 52 therein), or the life cycle may be
metagenic (i.e. with sexual and asexual generations) but without any significant test dimorphism.
These issues cannot be resolved at present. We note, however, that the life cycles of foraminifera are
highly diverse and may vary within one species according to the environmental conditions. For example,
in Allogromia laticollaris, some of the asexual pathways are related to diet (Lee et al., 1969), suggesting
that life cycles can be quite adaptive (Lee et al., 1991).
4.6. Geological implication
Our observations support the conclusions of Pawlowski (1991): some tiny deep-sea foraminiferal species
are virtually confined to sediment residues ⬍63 µm and may be useful in palaeoceanographic reconstructions. At the PAP site, Stainforthia sp. appears to have an ecology similar to that of Epistominella exigua.
It can be regarded as another ‘phytodetritus species’, an opportunist typical of areas with a seasonally
pulsed input of phytodetritus to the seafloor (Gooday, 1993). Such species can be used to recognise seasonally-pulsed organic matter inputs in the palaeoceanographic record (Smart, King, Gooday, Murray, &
Thomas, 1994; Thomas, Booth, Maslin, & Shackleton, 1995; Thomas & Gooday, 1996; Gooday, 1996).
Test morphology currently provides the only basis for separating species preserved in the fossil record.
The recent discovery of genetically distinct but morphologically convergent (i.e. cryptic) benthic foraminiferal species (Pawlowski et al., 1995; Kitazato, Tsuchiya, & Takahara, 2000) creates difficulties for
micropalaeontologists restricted to working with fossil material. Our study indicates that a detailed examination may reveal slight but consistent morphological differences between forms that at first sight appear
identical. These differences, which are also evident in cryptic metazoan species (Todaro, Fleeger, Hu,
Hrinevich, & Foltz, 1996; France & Kocher, 1996), offer the possibility to distinguish such species in the
fossil record.
5. Concluding remarks
We conclude that two taxonomically distinct but morphologically very similar Stainforthia species exist
in the deep NE Atlantic: Stainforthia fusiformis is predominantly a coastal species, but extends into the
bathyal zone (⬍3000 m) whereas Stainforthia sp. is confined to abyssal depths (⬎4000 m). Both are typical
opportunists that thrive in organically-enriched habitats separated by several kilometres in depth. We suggest that their similar lifestyles explain the remarkable morphological convergence between these two
species. It is presumably the availability of labile organic matter (phytodetrital aggregates) that allows
Stainforthia sp. to survive in the otherwise oligotrophic abyssal deep sea.
A comparison at the genetic (molecular) level would help to confirm our conclusion that the abyssal
and non-abyssal forms are distinct species. Assuming that they are distinct, then we need to establish
whether they are closely related or whether they belong to unrelated but morphologically convergent lineages. Such issues have a bearing on how foraminiferal species are defined and on the scale of their
geographical and bathymetric distributions. Obvious questions concern whether minor differences in test
morphology are underlain by more substantial genetic divergences and whether a greater degree of genetic
divergence exists between bathymetrically (vertically) separated populations or between geographically
(horizontally) separated populations. A combination of genetic and morphological studies is the only way
to approach such problems.
A.J. Gooday, E. Alve / Progress in Oceanography 50 (2001) 261–283
279
6. Taxonomic notes
6.1. Stainforthia fusiformis (Williamson)
Bulimina pupoides var. fusiformis Williamson, 1858, p. 63, pl. 5, Figs. 129–130.
‘Bulimina’ fusiformis (Williamson); Höglund, 1947, p. 232–235, Pl. 20, Fig. 3; text-Figs. 219–233.
Fursenkoina fusiformis (Williamson); Murray, 1971, p. 185, pl. 77, Figs. 1–5.
Virgulina fusiformis (Williamson): Parker, 1952, p. 417, pl. 6, Figs. 2–3.
Virgulinella fusiformis (Williamson); Atkinson, 1970, p. 395.
‘Stainforthia’ fusiformis (Williamson); Haynes, 1973, p. 124–125, Pl. 5, Figs. 7,8.
Cassidella fusiformis (Williamson); Lagoe, 1977, p.127, Pl. 4, Fig. 5.
Stainforthia fusiformis (Williamson); Alve, 1990, pl. 2, Fig. 17.
Stainforthia fusiformis (Williamson); Barmawidjaja, Jorissen, Puskaric, and Van der Zwaan, 1992, pl.
3, Figs. 1–4 (not 5).
Stainforthia fusiformis (Williamson); Nordberg, Gustafsson, and Krantz, 2000, Fig. 3(9).
6.1.1. Generic placement
This species has been placed in at least six genera with most recent authors favouring Stainforthia (see
selective synonomy above). According to Loeblich and Tappan (1964, 1987), Fursenkoina has an optically
granular wall structure while Stainforthia has a radial wall structure. In Stainforthia fusiformis the wall
structure is clearly radial. However, some authors (Haynes, 1990; Revets, 1996), consider this character
to have no taxonomic value at the generic level. We therefore assign this species to Stainforthia based on
the following characters:
1.
2.
3.
4.
the overall test morphology,
the location of the aperture in a marked depression,
the arch-like aperture rather than the narrow elongate aperture developed in Fursenkoina, and
the toothplate-like structure which forms a curved, denticulate lip partly bordering the aperture
(Loeblich & Tappan 1964, 1987; Haynes, 1981; Revets, 1996).
6.1.2. Apertural features
Differences in the shape and position of the aperture in Stainforthia fusiformis have caused taxonomic
confusion. The presence of a terminal aperture in adult individuals has commonly been used to distinguish
this from other Stainforthia species. Höglund (1947), however, reported that only 60–80% of specimens
possessed a terminal aperture. He provided the following detailed description. “In the adolescent test the
aperture is interio-marginal and consists of a very small, semicircular opening at the inner margin of the
apertural face, which is horseshoe-shaped and deeply excavated, the curved part of the apertural border
being provided with a comb-like lip directed outwards; in the adults the aperture is terminal, narrowly
ovate, with a collar on one side, and on the other a descending, double-folded tongue, whose free shank
is comb-like in its upper portion, the tongue not reaching the foramen of the preceding, adolescent chamber”
(Höglund, 1947, p. 232 therein). Clearly, therefore, this species includes specimens with terminal and nonterminal apertures. Höglund’s observations are confirmed by broken specimens which reveal the presence
of both kinds of aperture in one individual (Pl. 4, Fig. B).
280
A.J. Gooday, E. Alve / Progress in Oceanography 50 (2001) 261–283
6.1.3. Williamson’s syntypes
The syntype slide [Natural History Museum, London, registration number (18)96.8.13.28] contains about
112 specimens of S. fusiformis, disregarding those that clearly belong to other species. There is no locality
information appended, and so the slide is presumed to contain a mixture of specimens from the localities
mentioned in the text, namely Boston and March (both in Lincolnshire), Exmouth (Devon) and dredged
sands from Arran, Skye and the Shetland Islands (Williamson, 1858, p. 64 therein). The collection exhibits
the morphological variability typical of this species, particularly regarding the degree of elongation of the
test. In 7–8 specimens, the proximal chambers protrude beneath the bulbous distal chambers as the taillike feature noted above in some Norwegian specimens. The position of the aperture is variable. It is
located more or less terminally in 52 specimens and on the side of the final chamber in 15 specimens.
The aperture is not clearly visible in the remaining cases. The syntypes closely resemble the Norwegian
material examined for the present paper.
6.1.4. Material of Millett
As far as we are aware, Millett (1900) is the only author to have reported Stainforthia fusiformis from
the Indo-Pacific. One of his slides housed in the NHM, London (registration number 1956.6.27.298-301)
purports to contain specimens from his Stations 2, 6, 7, 14, 19, 27 and 30 in the Malay Archipelago. These
stations are not accurately localised but, like most of Millett’s localities, were situated in ‘shallow water
close inshore’ probably in about 12–14 fathoms (22–26 m) (Durrand, 1898). The slide contains only 5
obvious specimens and these are not easy to see clearly. Three look fairly similar to Williamson’s (1858)
syntypes and one seems to have a proximal ‘tail’. However, the chambers are rather more bulbous and
the sutures more strongly depressed than in the syntypes. The slit-like aperture evident in Millett’s figure
(1900, Pl. 2, Fig. 2 therein) is not apparent in any of these specimens. The remaining two specimens on
the slide do not closely resemble S. fusiformis.
6.2. Stainforthia sp.
Bulimina sp., Gooday, 1988, p. 71.
Fursenkoina sp.; Pawlowski and Lapierre, 1988, Pl. 1, Figs. 4 a,b.
Fursenkoina sp.; Pawlowski, 1991, p. 168, Pl. 1, Figs. 5a, 5b.
Fursenkoina sp.; Gooday, 1993, p. 200, Fig. 3 (size distribution).
Fursenkoina sp.; Gooday et al., 1995, Pl.1, Fig. A.
Fursenkoina sp.; Gooday, 1996, p. 1400, 1403.
6.2.1. Generic placement
This species differs from typical members of Stainforthia in several respects: the depressed area around
the aperture is not well developed, the toothplate is never clearly denticulate, and the chambers do not
exhibit the rather elongated form that is typical of fully-grown specimens of this genus. Nevertheless, the
wall structure is radial and the overall test morphology is very similar to that of S. fusiformis. We therefore
place it provisionally in Stainforthia. Note that the internal toothplate structure, which Revets (1996) suggested is a crucial character in Stainforthia, could not be examined in our abyssal specimens because of
their minute size.
Acknowledgements
This paper benefited considerably from discussions with Hiroshi Kitazato and his comments on the
manuscript. We also thank John Murray, Sue Goldstein, David Billett, and the reviewers, Stephen Culver
A.J. Gooday, E. Alve / Progress in Oceanography 50 (2001) 261–283
281
and Frans Jorissen, for their helpful comments, Bill Austin for the loan of specimens from the Iceland
Basin, Chris Smart for providing some of the scanning electron micrographs (Pl. 2, Figs. A–C), John
Whittaker for taxonomic advice and access to the collections of the Natural History Museum, and Mike
Conquer for help with the electronic manipulation of the photographic images. AJG is partly supported
by the European Union under the Marine Science and Technology Programme (MAST III), contract MAS3CT95-0018.
References
Alve, E. (1990). Variations in estuarine foraminiferal biofacies with diminishing oxygen conditions in Drammensfjord, SE Norway.
In C. Hemleben, M. A. Kaminski, W. Kuhnt, & D. B. Scott, Paleoecology, biostratigraphy, paleoceanography and taxonomy of
agglutinated foraminifera (pp. 661–694). The Netherlands: Kluwer Academic Publishers.
Alve, E. (1994). Opportunistic features of the foraminifer Stainforthia fusiformis (Williamson): evidence from Frierfjord, Norway.
Journal of Micropalaeontology, 13, 24.
Alve, E. (1995). Benthic foraminiferal distribution and recolonization of formerly anoxic environments in Drammensfjord, southern
Norway. Marine Micropaleontology, 25, 169–186.
Alve, E. (1999). Colonisation of new habitats by benthic foraminifera: a review. Earth Sciences Reviews, 46, 167–185.
Alve, E., & Murray, J. W. (2001). Temporal variability in vertical distributions of live (stained) intertidal foraminifera, southern
England. Journal of Foraminiferal Research, 31, 12–24.
Atkinson, K. (1970). The marine flora and fauna of the Isles of Scilly: foraminifera. Journal of Natural History, 4, 387–398.
Austin, W. E. N., & Evans, J. R. (2000). North East Atlantic benthic foraminifera: modern distribution patterns and palaeoecological
significance. Journal of the Geological Society, London, 157, 679–691.
Barnett, P. R. O., Watson, J., & Connelly, D. (1984). A multiple corer for taking virtually undisturbed samples from shelf, bathyal
and abyssal sediments. Oceanologica Acta, 7, 401–408.
Barmawidjaja, D. M., Jorissen, F. J., Puskaric, S., & Van der Zwaan, G. J. (1992). Microhabitat selection by benthic foraminifera
in the Northern Adriatic Sea. Journal of Foraminiferal Research, 22, 297–317.
Bernhard, J. M., & Bowser, S. S. (1999). Benthic foraminifera in dysoxic sediments: chloroplast sequestration and functional morphology. Marine Micropaleontology, 46, 149–165.
Bergsten, H. (1994). Recent benthic foraminifera of a transect from the North Pole to the Yermak Plateau, eastern central Arctic
Ocean. Marine Geology, 119, 251–267.
Biscaye, P. E., Kolla, V., & Turekian, K. K. (1976). Distribution of calcium carbonate in surface sediments of the Atlantic Ocean.
Journal of Geophysical Research, 81, 2595–2603.
Billett, D. S. M. (1991). Deep-sea holothurians. Oceanography and Marine Biology Annual Review, 29, 259–317.
Boltovsky, E., & Wright, R. (1976). Recent foraminifera. The Hague: W. Junk.
Campos-Creasey, L. C., Tyler, P. A., Gage, J. D., & John, A. W. G. (1994). Evidence for coupling the vertical flux of phytodetritus
to the diet and seasonal life history of the deep-sea echinoid Echinus affinis. Deep-Sea Research, 41, 369–388.
Caralp, M., Lamy, A., & Pujos, M. (1970). Contribution à la connaissance de la distribution bathymétrique des Foraminifères dans
le Golfe de Gascogne. Revista Española de Micropaleontologı́a, II, 55–84.
Creasey, S. S., & Rogers, A. D. (1999). Population genetics of bathyal and abyssal organisms. Advances in Marine Biology, 35, 1–151.
Darling, K. F., Kroon, D., Wade, C. M., & Leigh, A. J. (1996). Molecular phylogeny of the planktic foraminifera. Journal of
Foraminiferal Research, 26, 324–330.
De Vargas, C., Norris, R., Zaninetti, L., Gibb, S. W., & Pawlowski, J. (1999). Molecular evidence for cryptic speciation in planktonic
foraminifers and their relation to oceanic provinces. Proceedings of the National Academy of Sciences USA, 96, 2864–2868.
Durrand, A. (1898). On anchor mud from the Malay Archipelago. Journal of the Royal Microscopical Society, 1898, 255–257.
Echols, R. J. (1971). Distribution of foraminifera in sediments of the Scotia Sea area, Antarctic waters. American Geophysical Union,
Antarctic Research Series, 15, 93–168.
Etter, R. J., Rex, M. A., Chase, M. C., & Quattro, J. M. (1999). A genetic dimension to deep-sea biodiversity. Deep-Sea Research
I, 46, 1095–1099.
France, S. C., & Kocher, T. D. (1996). Geographic and bathymetric patterns of mitochondrial 16S rRNA sequence divergence among
deep-sea amphipods. Eurythenes gryllus. Marine Biology, 126, 633–643.
Gary, A. C., Healy-Williams, N., & Ehrlich, R. (1989). Water–mass relationships and morphologic variability in the benthic foraminifer Bolivina albatrossi Cushman, northern Gulf of Mexico. Journal of Foraminiferal Research, 19, 210–221.
Gary, A. C. (1991). Benthic foraminifera morphology: a tool for paleoenvironmental and paleowater depth interpretations. The American Association of Petroleum Geologists Bulletin, 75, 578.
282
A.J. Gooday, E. Alve / Progress in Oceanography 50 (2001) 261–283
Goldstein, S. T. (1999). Foraminifera: a biological overview. In B. K. Sen Gupta, Modern foraminifera (pp. 37–55). Dordrecht:
Kluwer Academic Publishers.
Gooday, A. J. (1988). A response by benthic foraminifera to the deposition of phytodetritus in the deep sea. Nature, London, 332,
70–73.
Gooday, A. J. (1993). Deep-sea benthic foraminiferal species which exploit phytodetritus: characteristic features and controls on
distribution. Marine Micropaleontology, 22, 187–205.
Gooday, A. J. (1996). Epifaunal and shallow infaunal foraminiferal communities at three abyssal NE Atlantic sites subject to differing
phytodetritus input regimes. Deep-Sea Research I, 43, 1395–1421.
Gooday, A. J., Carstens, M., & Thiel, H. (1995). Micro- and nanoforaminifera from abyssal northeast Atlantic sediments: a preliminary
report. Internationale Revue gesampten Hydrobiologie, 80, 361–383.
Gooday, A. J., & Lambshead, P. J. D. (1989). The influence of seasonally deposited phytodetritus on benthic foraminiferal populations
in the bathyal northeast Atlantic: the species response. Marine Ecology Progress Series, 58, 53–67.
Gooday, A. J., Levin, L. A., Linke, P., & Heeger, T. (1992). The role of benthic foraminifera in deep-sea food webs and carbon
cycling. In G. T. Rowe, & V. Pariente, Deep-sea food chains and the global carbon cycle (pp. 63–91). Dordrecht: Kluwer
Academic Publishers.
Gooday, A. J., & Turley, C. M. (1990) Responses by benthic organisms to inputs of organic material to the ocean floor: a review.
Philosophical Transactions of the Royal Society of London, A331, 119–138.
Groot, J. J., Benson, R. N., & Wehmiller, J. E. (1995). Palynological, foraminiferal, and aminostratigraphic studies of Quaternary
sediments from the U.S. Middle Atlantic upper continental slope, continental shelf and coastal plain. Quaternary Science Review,
14, 17–49.
Haynes, J. R. (1973). Cardigan Bay Recent foraminifera. Bulletin of the British Museum Natural History (Zoology), 4, 1–145.
Haynes, J. R. (1981). Foraminifera. London: Macmillan.
Haynes, J. R. (1990). The classification of the foraminifera—a review of historical and philosophical perspectives. Journal of Palaeontology, 33, 503–528.
Hermelin, J. O. R., & Scott, D. B. (1985). Recent benthic foraminifera from the central North Atlantic. Micropaleontology, 31,
199–220.
Höglund, H. (1947). Foraminifera in the Gullmar Fjord and the Skagerak. Zoologiska Bidrag från Uppsala, 26, 3–328, Pls 1–32.
Huber, B. T., Bijma, J., & Darling, K. (1997). Cryptic speciation in the living planktonic foraminifer Globigerinella siphonifera.
Paleobiology, 23, 33–62.
Kitazato, H., & Tsuchiya, M. (1999). Why are foraminifera useful proxies for modern and ancient marine environments? Kagoshima
University Research Center for the Pacific Islands Occasional Papers, 32, 3–17.
Kitazato, H., Tsuchiya, M., & Takahara, K. (2000). Recognition of breeding populations in foraminifera: an example using the genus
Glabratella. Paleontological Research, 4, 1–15.
Lagoe, M. B. (1977). Recent benthic foraminifera from the central Arctic Ocean. Journal of Foraminiferal Research, 7, 106–129.
Lampitt, R. S. (1990). Directly measured rapid growth of a deep-sea barnacle. Nature, London, 345, 805–807.
Lee, J. J., Faber, W. W., Anderson, O. R., & Pawlowski, J. (1991). Life cycles of foraminifera. In J. J. Lee, & O. R. Anderson,
Biology of foraminifera (pp. 285–334). New York: Academic Press.
Lee, J. J., Muller, W. A., Stone, R. J., McEnery, M. E., & Zucker, W. (1969). Standing crop of foraminifera in sublittoral epiphytic
communities of a Long Island salt marsh. Marine Biology, 4, 44–61.
Lochte, K. (1992). Bacterial standing stock and consumption of organic carbon in the benthic boundary layer of the abyssal North
Atlantic. In G. T. Rowe, & V. Pariente, Deep-sea food chains and the global carbon cycle (pp. 1–10). Dordrecht: Kluwer
Academic Publishers.
Loeblich, A. R., & Tappan, H. (1964). Sarcodina, chiefly thecamoebians and Foraminiferida. In R. C. Moore, Treatise on invertebrate
paleontology, part C, 1–2. New York: Geological Society of America.
Loeblich, A. R., & Tappan, H. (1987). Foraminiferal genera and their classification, 1–2. New York: Van Nostrand Reinhold.
Longhurst, A. (1998). Ecological geography of the sea. New York: Academic Press.
Lundquist, J. L., Culver, S. J., & Standley, D. J. (1997). Foraminiferal and lithologic indicators of depositional processes in Wilmington
and South Heyes submarine canyons, U.S. Atlantic continental slope. Journal of Foraminiferal Research, 27, 209–231.
Lutze, G. F. (1980). Depth distribution of benthic foraminifera on the continental margin off NW Africa. ‘Meteor’ ForschungsErgebnisse C, 32, 31–80.
Millett, F. W. (1900). Report on the recent foraminifera of the Malay Archipelago collected by Mr. A. Durrand, F.R.M.S.—part VIII.
Journal of the Royal Microscopical Society, 1900, 273–282.
Murray, J. W. (1963). Ecological experiments on Foraminiferida. Journal of the Marine Biological Association of the United Kingdom,
43, 621–642.
Murray, J. W. (1971). An atlas of British recent foraminiferids. London: Heinemann.
Murray, J. W. (1991). Ecology and palaeoecology of benthic foraminifera. Harlow: Longman Scientific and Technical.
A.J. Gooday, E. Alve / Progress in Oceanography 50 (2001) 261–283
283
Murray, J. W. (1992). Distribution and population dynamics of benthic foraminifera from the southern North Sea. Journal of Foraminiferal Research, 22, 114–128.
Nordberg, K., Gustafsson, M., & Krantz, A.-L. (2000). Decreasing oxygen concentrations in the Gullmar Fjord, Sweden, as confirmed
by benthic foraminifera, and the possible association with NAO. Journal of Marine Systems, 23, 303–316.
Ohga, T., & Kitazato, H. (1997). Seasonal changes in population ecology of bathyal foraminiferal populations in response to the flux
of organic matter (Sagami Bay, Japan). Terra Nova, 9, 33–37.
Parker, F. L. (1952). Foraminifera species off Portsmouth, New Hampshire. Bulletin Museum of comparative Zoology Harvard, 106,
391–423.
Pawlowski, J. (1991). Distribution and taxonomy of some benthic tiny foraminifers from Bermuda Rise. Micropaleontology, 37,
163–172.
Pawlowski, J., Bolivar, I., Farhni, J., & Zaninetti, L. (1995). DNA analysis of ‘Ammonia beccarii’ morphotypes: one or more species?
Marine Micropaleontology, 26, 171–178.
Pawlowski, J., & Lapierre, L. (1988). Recent benthic foraminifera from the north-east Atlantic. Revue de Paléontologie, 2, 873–878.
Pawlowski, J., Lee, J. J., & Gooday, A. J. (1993). Microforaminifera—perspective on a neglected group of foraminifera. Archiv für
Protistenkunde, 143, 271–284.
Pfannkuche, O. (1993). Benthic response to the sedimentation of particulate organic matter at the BIOTRANS station 47°N, 20°W.
Deep-Sea Research II, 40, 135–149.
Pfannkuche, O. (1992). Organic carbon flux through the benthic community in the temperate northeast Atlantic. In G. T. Rowe, &
V. Pariente, Deep-sea food chains and the global carbon cycle (pp. 183–198). Dordrecht: Kluwer Academic Publishers.
Pflum, C. E., & Frerichs, W. E. (1976). Gulf of Mexico deep-water foraminifers. Cushman Foundation for Foraminiferal Research
Special Publication, 14, 1–124.
Revets, S. A. (1996). The generic revision of the Bolivinitidae Cushman, 1927. Cushman Foundation Special Publication, 34, 1–55.
Scott, D. B., & Vilks, G. (1991). Benthonic foraminifera in the surface sediments of the deep-sea Arctic Ocean. Journal of Foraminiferal Research, 21, 20–38.
Smart, C. W., King, S. C., Gooday, A. J., Murray, J. W., & Thomas, E. (1994). A benthic foraminiferal proxy of pulsed organic
matter paleofluxes. Marine Micropaleontology, 23, 89–99.
Snider, L. J., Burnett, B. R., & Hessler, R. R. (1984). The composition and distribution of meiofauna and nanobiota in a central
North Pacific deep-sea area. Deep-Sea Research, 31, 1225–1249.
Somero, G. N. (1991). Adaptations to high hydrostatic pressure. Annual Review of Physiology, 54, 557–577.
Somero, G. N. (1992). Biochemical ecology of deep-sea animals. Experimentia, 48, 537–543.
Somero, G. N., Siebenaller, J. F., & Hochachka, P. W. (1982). Biochemical and physiological adaptations of deep-sea animals. In
G. T. Rowe, The sea, 8 (pp. 262–339). New York: Wiley Interscience.
Swallow, J. E., & Culver, S. J. (1999). Living (rose Bengal stained) benthic foraminifera from New Jersey continental margin canyons.
Journal of Foraminiferal Research, 29, 104–116.
Tendal, O. S., & Hessler, R. R. (1977). An introduction to the biology and systematics of Komokiacea (Textulariina Foraminiferida).
Galathea Report, 14, 165–194.
Thomas, E., Booth, L., Maslin, M., & Shackleton, N. J. (1995). Northeastern Atlantic benthic foraminifera during the last 45,000
years: changes in productivity seen from the bottom up. Paleoceanography, 10, 545–562.
Thomas, E., & Gooday, A. J. (1996). Cenozoic deep-sea benthic foraminifera: tracers for changes in oceanic productivity. Geology,
24, 355–358.
Todaro, M. A., Fleeger, J. W., Hu, Y. P., Hrinevich, A. W., & Foltz, D. W. (1996). Are meiofaunal species cosmopolitan? Morphological and molecular analysis of Xenotrichula intermedia (Gastrotricha: Chaetonotidae). Marine Biology, 125, 735–742.
Williamson, W. C. (1858). On the Recent foraminifera of Great Britain. London: Ray Society.
Wollenburg, J. E. (1992). Taxonomic notes on Recent benthic foraminifera in the Nansen Basin, Arctic Ocean. Berichte zur Polarforschung, 112, 1–137.
Wollenburg, J. E., & Mackensen, A. (1998a). Living benthic foraminifers from the central Arctic Ocean: faunal composition, standing
stock and diversity. Marine Micropaleontology, 34, 153–185.
Wollenburg, J. E., & Mackensen, A. (1998b). On the vertical distribution of living (Rose Bengal stained) benthic foraminifers in the
Arctic Ocean. Journal of Foraminiferal Research, 28, 268–285.