Agglutinated foraminifera (superfamily Hormosinacea) across the Indian margin oxygen minimum zone (Arabian Sea)

Abstract

We present a semi-quantitative survey of ‘live’ (stained) and dead hormosinacean foraminifera at six sites (500–2,000 m water depth; bottom-water oxygen concentrations 0.007–2.43 ml L⁻¹) across the Indian margin oxygen minimum zone (OMZ). Abundance of stained and dead specimens was highest at 800 m followed by 1,100 m, lowest at 2,000 m (stained) and 500 m (dead). The peak at 800 m possibly represents a release from oxygen stress combined with a rich food supply (‘edge effect’). We recognised 31 species (27 Reophax, 2 Hormosinella, 1 Hormosina and 1 Nodosinella) among the 605 stained and dead specimens; the majority (21) are apparently undescribed. Species richness was low at 2,000 m; within the OMZ, it was maximal at 1,100 m and minimal at 500 m for both stained and dead populations. Three species (R. agglutinatus, R. aff. bilocularis and R. dentaliniformis) occurred across the entire depth range. However, most species were either confined to the 2,000-m site or to one or more sites within the OMZ. Multivariate analysis of assemblage composition revealed that the 2,000-m site was distinct from shallower sites. Within the OMZ, the 900- and 1,100-m sites were the most similar, and the 500-m site the most distinct. Stained:dead test ratios were maximal at 500–835 m, perhaps reflecting enhanced preservation of cytoplasm at very low oxygen concentrations. At least two Reophax species are common to the Indian and Pakistan margin OMZ; one of these may be confined to the core of the Arabian Sea OMZ.

Appendix 1: Species descriptions

The following section provides brief descriptions of the species recognised in this study. Some species originally assigned to Reophax have been assigned to other genera by later authors (e.g. R. dentaliniformis to Hormosina and Nodulina). For simplicity, we have adopted a conservative approach by retaining the majority of our species in the genus Reophax. Most are illustrated in Figs. 5, 6, 7, 8, 9, 10 and 11.

Fig. 7

Hormosinaceans from the Indian margin. SEM images (a, b, d, f, h, j); reflected light images (c, e, g, i). Hormosinella ovicula Brady, 1879; Dive 1098, 2,000 m (a). Nodosinella gaussica Rhumbler, 1913; Dive 1098, 2,000 m (b). Reophax agglutinatus Cushman, 1913; Dive 1101, 800 m (c, d). Reophax aff bilocularis Flint, 1899 (e, f). Dive 1101, 800 m. Reophax dentaliniformis Brady 1881; Dive 1101, 800 m (g, h). Reophax horridus Cushman, 1912; Dive 1101-2, 900m (i, j). All scale bars 500 μm

Fig. 8

Hormosinaceans from the Indian margin. Left-hand column reflected light images; right-hand column SEM images. Reophax aff. scorpiurus de Montfort, 1808, same specimen; Dive 1098, 2,000 m (a, b). Reophax aff spiculifer Brady, 1881, same specimen; Dive 1100, 900 m (c, d). Reophax sp. 1, same specimen; Dive 1099, 1,100 m (e, f). Reophax sp. 2; Dive 1101, 800 m (g, h). Reophax sp. 3; Dive 1099, 1,100 m (i, j). Reophax sp. 4 (the apertural neck appears to be damaged in this specimen); Dive 1099, 1,100 m (k, l). All scale bars 500 μm except where indicated otherwise

Fig. 9

Hormosinaceans from the Indian margin. Left-hand column reflected light images; right-hand column SEM images. In all cases, the same specimen has been illustrated using the two methods. Reophax sp. 5; Dive 1100, 900 m (a, b). Reophax sp. 6; Dive 1098, 2,000 m (c, d). Reophax sp. 7; Dive 1102, 500 m (e, f). Reophax sp. 8; Dive 1101, 800 m (g, h). Reophax sp. 9; Dive 1099, 1,100 m (i, j). All scale bars  500 μm

Fig. 10

Hormosinaceans from the Indian margin. Left-hand column reflected light images; right-hand column SEM images. Reophax sp. 10, same specimen; Dive 1101, 800 m (a, b). Reophax sp. 10A same specimen; Dive 1101, 800 m (c, d). Reophax sp. 11; Dive 1101, 800 m (e, f). Reophax sp. 12; Dive 1100, 900 m (g, h). Reophax sp. 13; Dive 1099, 1,100 m (i, j). Reophax sp. 14 same specimen; Dive 1099, 1,100 m (k, l). All scale bars 500 μm

Fig. 11

Hormosinaceans from the Indian margin. Left-hand column reflected light images; right-hand column SEM images. In all cases, the same specimen has been illustrated using the two methods. Reophax sp. 15; Dive 1101, 800 m (a, b). Reophax sp. 16; initial chamber lost during preparation for SEM; Dive 1099, 1,100 m (c, d). Reophax sp. 17; Dive 1100, 900 m (e, f). Reophax sp. 18; same specimen; Dive 1100, 900 m (g, h). Reophax sp. 19; Dive 1100, 900 m (i, j). Reophax sp. 20; Dive 1100–1, 835 m (k, l). All scale bars 500 μm

Superfamily Hormosinacea Haeckel 1894

Family Hormosinidae Haeckel 1894

Hormosinella distans (Brady, 1881)

Chambers ovate and well separated by thin neck. Wall very thin, composed of fine-grained material. All specimens in our material were broken. They resemble those illustrated by Brady (1884, pl. 31, figs. 18–22).

Hormosinella ovicula Brady, 1879

Fig. 7a

Chambers droplet-shaped with adjacent chambers separated by elongated necks. Apertural neck well defined. Test wall fine-grained. Length up to 1.7 mm. Our specimens resemble those illustrated by Brady (1879, pl. 4, fig. 6)

Hormosina globulifera Brady, 1879

Four to five large, globular chambers. Wall composed of fine-grained material. Terminal aperture located at end of narrow neck. Our specimens resemble those illustrated by Brady (1879, pl. 4, figs. 4 and 5).

Nodosinella gaussica Rhumbler, 1913

Fig. 7b

Large, robust species with flask-shaped chambers. Test fine-grained, well cemented, with a smooth outer surface. Length up to 2.25 mm. Our specimens resemble those illustrated by Zheng and Fu (2001, pl. 15, figs. 1, 2).

Reophax agglutinatus Cushman, 1913

Fig. 7c, d

Test large, compact, comprising 3 or more chambers increasing rapidly in size but largely obscured by the globigerinacean shells of which the wall is composed. In particular, the final two chambers are dominated by large Globorotalia shells. Coccoliths and other fine particles fill in the small spaces between the large particles. Gently tapered apertural neck made of small Globigerina shells distinctly developed. Length up to 2.25 mm.

Remarks A variety of test morphologies have been illustrated under this name. Our specimens resemble those illustrated by Zheng and Fu (2001, pl. 13, figs. 12a–13b). Schröder (1986, pl. 23, top left specimen from 2750 m depth in the NW Atlantic) illustrates a similar specimen as Reophax scorpiurus.

Reophax aff. bilocularis Flint, 1899

Fig. 7e, f

Test comprises two fairly well-rounded chambers, each longer than broad, and with the final chamber larger than initial chamber. Wall with fairly smooth surface, composed of coccoliths and small globigerinacean shells. Aperture located at end of short neck. Length up to 960 μm.

Remarks The name Reophax bilocularis has been applied to a variety of 2-chambered hormosinaceans with walls composed of different types of agglutinated particle. It probably represents a species complex rather than a single species. In our form, the test is asymmetrical about the longitudinal axis and there is no constriction between the two chambers. Several of the specimens from the North Carolina margin (1,423 m depth) illustrated by Flint (1899, pl. 17, fig. 2) are also not symmetrical, although the two chambers are more clearly delineated than in this Indian margin form. The only other similar species, R. subfusiformis Earland 1934, usually has 3–4 chambers, the final one being clearly tapered.

Reophax dentaliniformis Brady, 1881

Figs. 5a and 7g, h

Test slender, tapering, composed of up to 8 chambers arranged along a straight or curved axis. Final chamber typically elongate with more or less parallel sides. Wall made of coarse sand grains with relatively smooth outer surface and incorporating a few sponge spicules. Short cylindrical apertural neck. Length 1,030–1,550 μm.

Remarks Brönnimann and Whittaker (1980) placed Reophax dentaliniformis in Hormosina because of its symmetrical chambers, lack of an upturned “tail” and distinct neck. We follow Schröder (1986) and several other authors in retaining it within Reophax. Except for having more chambers, our Indian margin specimens are fairly similar to Brady’s (1884, pl. 30, figs. 21, 22) syntypes, one of which we illustrate in Fig. 5b for comparison. The photograph of R. aff. R. dentaliniformis, also from the Indian margin, in Zobel (1973, pl. 1, fig. 27) seems more similar to R. dentaliniformis of Larkin and Gooday (2009). The two specimens illustrated by Hermelin and Shimmield (1990, pl. 1, figs. 1–2) have fewer chambers than our specimens and the final chambers have a bulbous or tapered outline, rather than being parallel sided.

Reophax aff. horridus Cushman, 1912

Fig. 7i, j

Chambers globular and clearly differentiated from each other. Wall coarse-grained, composed of mineral grains with numerous randomly protruding sponge spicules, giving a bristly appearance. Terminal chamber tapers to an apertural neck made of same material as the rest of the test. Length up to 1,900 μm.

Remarks In specimens of Reophax horridus illustrated by both Cushman (1912, pl. 28, figs. 3, 4) and Schröder (1986, pl. 15, figs. 6, 7) the sponge spicules are all oriented in one direction (backwards). In the Indian margin specimens, however, the spicules are randomly oriented. This could reflect a species-level difference and our identification is therefore tentative.

Reophax aff. scorpiurus de Montfort, 1808

Fig. 8a, b

Test elongate and slender, comprising 4–6 fairly chambers that become more elongate distally. Most chambers with ventricose asymmetry (shorter on one side than on outer side); final chamber tapering into slender neck. Earliest chambers curved or angled upwards, producing scorpion-like proximal “flick”. Wall coarse-grained, composed of mineral grains with scattered sponge spicules. Length typically ∼1,000 μm.

Remarks Since Reophax scorpiurus was first described from Adriatic beach sands (Brönnimann and Whittaker 1980), the name has been applied to a wide range of forms from shallow and deep water, which almost certainly represent different species (e.g. Schröder 1986). One of the specimens illustrated by Schröder (1986, pl. 14, fig. 5) is fairly similar to our form, although it is more slender and originates from much deeper water. Reophax scorpiurus of Zobel (1973, pl. 1, fig. 54) from the Indian margin appears to be a different species.

Reophax aff. spiculifer Brady, 1879

Fig. 8c, d

Test elongate, more or less straight, comprising several slim chambers that increase in size distally. Walls composed of sponge spicules and fairly coarse-grained mineral particles. Terminal chamber elongate and tapering slightly to apertural neck. Small fragments of sponge spicules form ring around terminal aperture. Length typically ∼660 μm.

Remarks The chambers are similar in shape to those of Brady’s (1884, pl. 31, figs. 16, 17) species, but the wall incorporates mineral grains in addition to sponge spicules, and the spicules themselves are arranged less neatly than in Brady’s illustration. On the other hand, spicules are more numerous, and the chambers are more streamlined, than in Schiebel’s (1992, pl. 8, fig. 10) illustration.

Reophax species 1

Fig. 8e, f

Test composed of 4 or more approximately spherical chambers, fairly well differentiated from one another and arranged along a slightly curved or nearly straight axis. Wall composed of heterogeneous mixture of mineral grains, intact and fragmentary radiolarians, and sponge spicules, resulting in highly irregular surface. Spaces between larger grains filled with coccoliths and other fine particles. Narrow but clearly-developed, parallel-sided apertural neck. Length typically ∼1,690 μm (Fig. 6a, b).

Remarks

This species most closely resembles Hormosina spiculifera Hofker 1972, from bathyal depths in the Caribbean but has less distinct sutures between the chambers and an even more irregular test surface due to the incorporation of radiolarian tests into the wall.

Reophax species 2

Fig. 8g, h

Test comprises 3 chambers arranged along a straight axis and increasing in size distally; the final chamber is flask-shaped with relatively large aperture. Wall coarse-grained, composed of a mixture of mineral grains and projecting sponge spicules giving the test a bristly appearance. Most spicules are directed backwards. Length ∼1,200 μm.

Reophax species 3

Fig. 8i, j

Test comprises at least 4 chambers arranged along a straight axis and increasing gradually in size. Wall composed of a wide variety of particles, including mineral grains, radiolarian and sponge spicule fragments with fine-grained material dominated by coccoliths filling the interstices between the larger grains. Apertural neck fairly wide and well developed, composed mainly of smaller mineral grains. Length typically ∼1,000 μm.

Reophax species 4

Figs. 5e and 8k, l

Test composed of 6–7 rounded, clearly-defined chambers. Test coarse-grained and consisting mainly of mineral grains with occasional protruding sponge spicules. Aperture at end of short neck composed of finer-grained material than rest of test. Length 1,100–1,500 μm.

Reophax species 5

Fig. 9a, b

Test comprises at least 3 slender, flask-shaped chambers arranged along a more or less linear axis. Wall made of fairly small mineral grains and sponge spicules set in a fine-grained matrix. Most of the spicules are flat-lying and do not protrude from the wall. Terminal chamber tapers into a slender apertural neck. Length 600 μm.

Remarks The flask-shaped, clearly delimited chambers distinguish this species from R. spiculifer.

Reophax species 6

Fig. 9c, d

Test with at least 4 chambers arranged on a linear axis. Chambers are rather globular but closely abutting; apertural neck not developed. Wall fairly coarse-grained, composed of mineral grains and flat-lying sponge spicules. Length ∼1,220 μm.

Reophax species 7

Figs 6a, 9e, f

Test comprises 3 or more indistinct chambers, arranged along a more or less linear axis. Final chamber tapers to distinct apertural neck. Wall muddy-brown in colour, fine-grained, composed of coccoliths and clay particles. Length ∼1,180 μm.

Remarks This species is identical to Reophax sp. 2 of Larkin and Gooday (2009), which is common at 300 m depth on the Pakistan margin.

Reophax species 8

Fig. 9g, h

Test comprises 4–5 bulbous and fairly distinct chambers. The final flask-shaped chamber tapers to short, fairly wide apertural neck. Wall composed of globigerinacean shells set in matrix of fine-grained particles with scattered, proximally directed sponge spicules. Length ∼1,920 μm.

Reophax species 9

Fig. 9i, j

Test composed of 6 chambers that are not clearly differentiated on the test exterior. Wall appears “muddy” under light microscope, composed of fairly large mineral grains embedded in a matrix consisting mainly of coccoliths. Prominent apertural neck composed of finer-grained material than rest of test. Terminal aperture with fine-grained flange. Length 1,500 μm.

Remarks This species resembles R. helenae (Rhumbler 1911) of Schröder (1986, pl. 15, fig. 8), from the abyssal NE Atlantic (4,180–5,779 m) and Timm (1992, pl. 2, fig. 5) from the Gulf of Guinea (3,987–4,970 m), but is rather more elongate with the widest point closer to the distal end and a shorter apertural neck. According to the original description (Rhumbler 1911), based on material collected at >4,000 m depth off St Vincent in the Caribbean, R. helenae has a test composed of large planktonic foraminiferal shell fragments, very different from the wall structure of the present species.

Reophax species 10

Fig. 10a, b

Test slender and delicate, composed of 4–5 poorly-defined chambers arranged along gently curved axis and increasing in size towards elongate final chamber, which merges into the apertural neck. Wall composed mainly of larger and smaller globigerinacean shells (many damaged or slightly dissolved) that tend to obscure the chamber shape. Fine-grained material (mainly coccoliths) fills the small spaces between the planktonic shells. Length ∼960 μm.

Remarks This fairly common species is similar in general form to Reophax aff. scorpiurus of the present study but has a completely different test wall composition (globigerinacean shells rather than mineral grains and sponge spicules). It also lacks the upturned early chambers of typical ‘Reophax scorpiurus’ morphotypes.

Reophax species 10A

Fig. 10c, d

Remarks This single specimen (length 1,040 μm) is probably a shorter and relatively wider variant of Reophax sp. 10, which it resembles in wall structure as well as general morphology. However, it is treated as a distinct form for the purposes of the present study.

Reophax species 11

Fig. 10e, f

Test comprising 2 chambers that tend to be more inflated than those of R. sp. 10. Final chamber produced into apertural neck composed of juvenile globigerinacean shells. Remainder of test wall consists of mainly small, but also scattered larger, globigerinacean shells with little intervening matrix. Length 770 μm.

Remarks The status of this bilocular form requires further investigation. At least some examples have broken proximal ends and probably represent incomplete specimens of Reophax sp. 10, which they closely resemble in wall structure and composition. However, in others, including the figured specimens, the proximal end is complete, suggesting that they may represent a distinct species.

Reophax species 12

Fig. 10g, h

Test comprising 2 rather bulbous, flask-shaped chambers (the proximal ends of the illustrated specimens are intact). Wall consists of larger and smaller globigerinacean shells with a few randomly arranged sponge spicules. Apertural neck not clearly developed. Length 1,460 μm.

Remarks This rare species differs from Reophax aff. bilocularis in having two chambers separated by a clearly developed constriction and a completely different test wall composition. It is about twice as large as the other bilocular form, Reophax sp. 11, from which it also differs in having a wall that incorporates sponge spicules as well as globigerinacean shells. It resembles R. bilocularis morphotype A of Fontanier et al. (2013, fig. 3.2) from much deeper water (2,974 m) on the Namibian margin, although the chambers are rather more elongate than the Namibian form.

Reophax species 13

Fig. 10i, j

Test slender, curved or straight consisting of up to 8 reasonable well-defined chambers, sometimes with upturned initial chambers as in R. scorpiurus. Wall consists mainly of larger and smaller planktonic foraminiferal shells with little intervening fine-grained material. Some dissolution of these planktonic shells is evident. Short cylindrical apertural neck composed of finer-grained material (mineral grains) than the rest of the test. Length ∼2,100 μm.

Remarks Larger and relatively wider than Reophax sp. 10 with rather more clearly-defined chambers composed entirely of globigerinacean shells, giving the test a ‘cleaner’, more uniform appearance. The chambers, particularly the final one, are more bulbous than those of R. sp. 10 and 10A.

Reophax species 14

Fig. 10k, l

Test elongate, comprising 5–6 chambers arranged along a curved axis; their shape is obscured by the mixture of larger and smaller planktonic foraminiferan shells of which the wall is constructed. A few benthic tests are also incorporated, and fine-grained material dominated by coccoliths fills spaces between the large particles. Long, cylindrical apertural neck composed of juvenile globigerinacean shells and with fine-grained rim around terminal aperture. Length ∼1,600 μm.

Remarks Larger and more robust than Reophax sp. 10 and with a more distinct apertural neck. Compared with R. sp. 10, the wall is composed of a more heterogeneous mixture of smaller and larger globigerinacean shells, which include flat Globorotalia tests.

Reophax species 15

Fig. 11a, b

Test elongate comprising 4–5 chambers arranged along a straight or slightly curved axis. Wall a very heterogeneous mixture of larger and smaller globigerinacean shells. Relatively short apertural neck made of small globigerinacean shells. Length 1,600–1,700 μm.

Remarks Similar to Reophax sp. 10 in general shape but considerably larger, straighter, and with a more irregular appearance due to the incorporation of large shells into the test wall. In both these respects it resembles R. sp. 14 but the test is straight rather than curved and lacks the distinctive neck of that species.

Reophax species 16

Fig. 11c, d

Test with 2–3 chambers arranged on a straight axis. Chambers globular and well differentiated, each tapering towards the next chamber. Wall composed mainly of globigerinacean shells and sponge spicules. Final chamber tapers into a long apertural neck made from progressively finer-grained material, including some juvenile planktonic shells. Length ∼1,700 μm.

Reophax species 17

Fig. 11e, f

Test with up to 4 chambers arranged along a slightly curved axis and ranging in shape from spherical at the proximal end to flask-shaped at the distal end. Final chamber produced into a pronounced apertural neck composed of small juvenile globigerinacean shells grading into finer mineral particles and ending in a distinctive flange, formed of very fine particles. Main part of test wall composed of globigerinacean shells and shell fragments together with sponge spicules and occasional benthic foraminiferal tests and radiolarian fragments. Some dissolution of globigerinacean shells observed. Length ∼1,550 μm.

Reophax species 18

Fig. 11g, h

Test comprising 3 chambers arranged on a linear axis. Wall composed of globigerinacean shells set in a fine-grained matrix composed mainly of coccoliths. Final chamber flask-shaped, tapering to a distinct apertural neck made of finer-grained material than the rest of the test. Length 1,400 μm.

Reophax species 19

Fig. 11i, j

Test compact, comprising 2 chambers arranged on a linear axis. Final chamber appears flask-shaped. However, both chambers are obscured by the very coarsely agglutinated wall, which is composed of a jumble of larger and smaller globigerinacean shells and large shell fragments with little intervening fine-grained matrix. Scattered sponge spicules, most directed backwards, protrude from wall. Apertural neck relatively short, broad and cylindrical and composed of fine mineral grains. Length ∼1,400 μm.

Remarks It is possible that this form is a variant of Reophax species 18. It requires further study.

Reophax species 20

Fig. 11k, l

Test comprises 2 or more slender, indistinct chambers, arranged on a straight or slightly curving axis. Wall composed of globigerinacean shells that are set into the wall and do not project to any significant extent. As a result, the wall appears white and shiny under the light microscope. Terminal chamber tapers to an apertural neck which is made of finer-grained juvenile globigerinacean shells. Length ∼1,000 μm.