Emendation of the foraminiferal genus Cribrostomoides Cushman, 1910, and its taxonomic implications

A review of the taxonomic history of the agglutinated (benthonic) foraminiferal genus Cribrostomoides Cushman, 1910 reveals much confusion concerning its type species, coiling mode and apertural characteristics. We believe the originally designated type species of Cribrostomoides Cushman, 1910, C. bradyi Cushman, 1910, to be no more than varietally (i.e. infra-subspecifically) distinct from, and therefore a junior synonym of, Haplophragmoides subglobosus Cushman, 1910. The coiling of Cribrostomoides, as typified by C. subglobosus (Cushman, 1910), is in the form of an involute streptospire characterised by a repeated alternation in axis. The aperture of the genus is equatorially or asymmetrically placed and interio-areal and single (in megalospheric and juvenile microspheric specimens) to areal and multiple (in microspheric adults). In order to stabilise the concept of Cribrostomoides, we have designated lectotypes for both C. bradyi and H. subglobosus, and have also emended the generic diagnosis of Loeblich and Tappan (1987). Criteria for the discrimination of Cribrostomoides emend, herein and allied genera are tabulated.


INTRODUCTION
The lituolid (agglutinated benthonic foraminiferal) genus Cushman, 1910 is an ubiquitous component of modern decp-sea faunas. It has also been reported by n u m e r o u s a u t h o r s from "flysch-type" foraminiferal assemblages of Late Cretaceous to Oligocene age.

CI.ibrostcimoidcs
Unfortunately, this widely cited genus does not benefit from having a well-defined description. There is much confusion in the literature concerning its type-species, coiling mode and apertural characteristics. This is partly attributable to the poor quality of the original illustrations, and to the fact that the original description was based solely upon the external morphology of the test. The purpose of t h e present s t u d y is to stabilise t h e concept of Cvibrostorrroidc~s based upon lectotypification of the type species (and emendation of the generic diagnosis). For this purpose w e have illustrated type specimens from the collections of J.A. Cushman, H.B. Brady, and G.O. Sars, and have dissected specimens to reveal the mode of coiling and wall structure

TAXONOMIC HISTORY OF THE GENUS CRIBROSTO-MODES CUSHMAN, I 9 I 0
In his "North Pacific Monograph', Cushman (1910: 108-109 ) first described the new genus Cribrostonioides, with the new species C. brridyi as the type. The type description for C. brailyi reads thus: "l'est free, planospiral, of several coils, chambered, the last-formed coil with several chambers progressively increasing in size, arenaceous wall, with much cement ... , aperture in young specimens a simple elongate slit at the base of the apertural face, later subdivided by tooth-like processes, and in the adult represented by a linear series of dialinct rounded [interio-areal or areal] openings." The type figures are reproduced in Fig. 1.la-c. I n his subsequent "North Atlantic Monograph", Cushman (1920: 52-54) acknowledged the possibility t h a t C r i b 1'0s to ni o ides b r a d y i might be s y n o n y m o u s w i t h H~7plophragmoides subglobosuni (Sars) ( s i c ) . However, h e retained t h e t w o as s e p a r a t e species, s t a t i n g t h a t "Cribrostoiiioides may be easily distinguished in the adult by the row of pores forming the aperture, while the aperture of H. wbglobosuni is always simple." In their studies of"'Upper Cretaceous" [Palaeocene] m'iterial from the Lizard Springs Formation of Trinidad, Cushman & Jarvis (1927, 1932 applied the generic name Cribrostornoides to a species ( C . tririitateiisis Cushman & Jarvis, 1927) characterised by multiple interio-marginal r'ither than interio-areal openings, in so doing implicitly emended the concept of the genus. In fact, "Crihrosfoirioides" trirritaterrsis appears distinct from Cribrostcnnoides S.S. in its 1 a-c  Fig. 1.1. Cribrostortioidrs subg/obosirs forma subylobosus (Cushman, 1910). x32. Reproduction of type figures of Haplophmginoidrs s.irlylobosirs Cushman, 1910, (Textfigs. 102-104). Textfig. 104 from Albatross Station D3603 (1771fm or 3241m). Fig. 1.2. Cribrostomoides siibgld~osiis forma subglobosirs (Cushman, 1910). x36. Lectotype of Haplophraginoides subglobosus Cushman, 1910 (herein designated).

. Cribrostowroides
The Foraminifera1 genus Cribrostoirroides inter i oma r g i 11 n 1 rat her than i n ter i o-ar e a 1 aperture (and from Barkerinn Frizzell & Schwartz, 1950 (where i t was placed by F r i u e l l & Schwartz (1950)) in its arenaceous rather than microgranular wall and in lacking internal partitions). We believe "C. trinitatensis" probably represents a separate genus. Hoglund (1947: 144-145) synonymised Cribrostomoides Cushman, 1910 with Labrospira t i . gen., apparently rejecting it on the grounds of the inappropriateness of the name (observing a complete gradation from specimens with simple slit-likc dpertures ("Lnkrospiva") to rare specimens with multiple apertures ("Cribrostotrioidrs") and arguing that Cushman was "...in no way justified ..." in "...singling out such specimens [as the latter] and setting them LIP ... as a... new g e n u s " ) . In fact, Articles 18 a n d 23m of the International Code of Zoological Nomenclature (Ride et a/., 1985) state that the "inappropriateness" of a name does not affect its avail'itdity, and that no valid available name can be rejected on tliis or any other ground. Moreover, Hoglund a I so s y no n y m i s e d the t y p es p e c i e s o f C v i b r 0 s to 111 o ides C u s h m a n , 1 9 10 (C. br17dyi C u s h m a n ) with Lobrospira ~t t h g l o h~~a ( C . O . Sars, 1871Sars, (1872) (sic), i n so doing, automaticall!, making Labra.;l~irn a junior synonym of Crihros toriroid?.s. Frizzell & Schwartz (1950: 3) emended Cribrosfonioides on the basis of i t s apertural characteristics, citing as typical a sirn ple "ellipt i cLi 1 or crescent-sha ped " slit, located "...slightly above ..." the base of the septa1 face and "...completely surrounded b y it...". 'They added that "provisionally, it seems advisable to regard b r d y i and sulylobosii as distinct spccics, each including variant individuals i n which multiple apertures are developed".
In their revised diagnosis of the genus, they stated the coiling mode to be "slightly streptospiral" in early stages, later becoming "planispiral and symmetrical", They further stated the aperture to be "equatorial, just above the base of the final chamber face, ,., a simple slit in the early chambers, later ... a linear series of irregular to rounded openings".

OBSERVATIONS ON THE GENUS CRIBROSTOMOIDES CLISHMAN, I 9 I 0
(1) On the type species The type species (by original designation) of the genus Crib ros t o irr o I dcs u n e q u i v o c a 11 y C u shin a ri, 1 9 1 0 is Cribrostomoides bradyi Cushman, 1910. Confusion arises from the arguable synonymy of C . bradyi Cushman, 1910 and C. subglobosus auctt.
The earliest citations of Lituola subglobosa (M. Sars, 1868Sars, (1869; G.O. Sars, 1871Sars, (1872; Brady, 1881a,b) a r e unaccompanied by figures or descriptions, and are invalid. The next citation (Brady, 1884) synonymised Lituola sub;:/obosa with the fossil species Haplopkragmiurn l a t i d o r s a t~i m Bornemann, which is herein regarded a s distinct a n d referable to the genus Hnplophvagrnoides Cushman, 1910. Interestingly, one of the slides in the Brady Collection in the Natural History Museum (BMNH) (which was evidently sent to Brady by Michael Sars) bears the pencilled inscription "Lituoln subglobosn" crossed out and rep 1 a c e d by the inked ins c r i p t i o n " H a p I o p 11 ra g m i ci W I latiiiorsatum" (see our Fig. 2.3). It follows that if Brady had used Sars' designation instead of trying to synonymise it under Bornemann's species, he would have validated szibgiobosa in his Challenger Report. Cushman (1910) was the first to validate the specific name sub;:/obosus, though at the time of writing he was evidently unaware of this. This is noted on an undated addendum slip in the Natural History Museum's edition of the  Cushman, 1910 were validated in the same publication (Cushman, 1910), the former species on p. 108 and the latter on p. 105.
The microfossil collections in the United States National Museum of Natural History, Smithsonian Institution, house about six trays of slides labelled "Cribrostoiiioides brati!/?' and "HiiiIlot7hragi~roides siibgl(~bos~is" from Albatross and Nero stations studied by Cushman (1910Cushman ( , 1920Cushman ( , 1921. The bulk of this material is from the North Atlantic (Cushman, 1920), but some is also from the North Pacific (Cushman, 1910) and some from the Philippines (Cushman, 1921). All of the p acific : -' (s\ ntypic) .
Hased partly o n a s t u d y of syntypic suites of both "species", we believe Cribrosf [?iiiOidc,s hradyi Cushman, 1910 (sce our Fig. 1.4,6; Fig. 2. and PI. 3) and Hn~Jlo~J/iraXriioides siiiiglobostis Cushman, 1910 (see our Fig. 1. 1-3, 5 and Pls. l,?) to be no more than infra-subspecifically distinct and thcrefore for practical purposes synonymous (Lukina (1980) rc,iched a similar conclusion). Forma brad!]; differs from forma sirbglobosiis essentially only in its size (being larger), a n d in its wall texture (being finer) a n d composition (apparently being selective in its use of mafic particles). Thc,se differences are interpreted as due to differences in substrate rather than genetic effects (i.e. phenotypic rather t h m genotypic).
Article 24 of the ICZN (Ride c'f al., 1985) (the "Principle of the First Reviser") states that "If two ... names are published specimens of both "species" are considered cotyyic Fig. 2. Syntypes of "Cribrostomoides bradyi" from t h e C u s h m a n Collection. Fig. 2
We accordingly assign precedence to Haplophragmoides subglobosus Cushman, 1910. This is the more widely used name and the one whose retention would best maintain nomenclatorial stability. It also has "position precedence" (defined as that "given to the the nominal species cited first in the work, page or line"). Recommendation 69B(Il) of the ICZN suggests that this be recognised in the event of "all other things being equal" (Ride et al., 1985).
(2) On the coiling mode The widely-held belief (e.g. of Cushman, 1910, Frizzell and Schwartz, 1950, and Loeblich & Tappan, 1964) that the chamber arrangement i n t h e g e n u s Cribrostomoides is planispiral is in our opinion untenable. This was first called into question by the work of Hoglund 1947: 144-145), who noted that Labrospira subglobosa (G.O. Sars) (sic) (which he regarded as a senior synonym of Cribrostomoides bradyi Cushman) "is not formed as a completely flat spiral", that "this is frequently plainly visible in the last volution, which is more o r less twisted" a n d that "the irregularity is particularly noticeable in the initial portion, where the arrangement of the chambers is difficult to determine in a section". Hoglund's figured section (Textfigure 126) seems to indicate that later whorls are arranged more or less at right angles to earlier ones. This kind of coiling conforms to that which Banner & Blow (1967) defined (in the case of the planktonic genus Pulleniatinu Cushman) as "streptospiral". Hofker (1976: 54-55) also observed of Cribrostomoides bradyi Cushman that "especially the early chambers are streptospirally arranged, so that in a section transverse to the last formed coil the whole spiral is seen, whereas in sections in t h e plane of t h e last formed coil, several chambers of the first coils are sectioned transversely". He erroneously added that Hoglund's subglobosa "does not show" the streptospiral initial part.

741).
Our dissected specimen of Cribrostomoides subglobosus forma subglobosus from the Cushman Collection (Pl. 1, fig. 4) confirms the suspected involute streptospiral coiling mode, characterised by a (repeated) alternation in axis. This is manifest by regular intersections by the plane of section of

Explanation of Plate 2
Metatypes of "Cribrostomoides bradyi" (specimens identified as such by J.A. Cushman). All specimens are from the Cushman Collection, USNM. Fig. la-3b. Cribrostomoides subglobosus forma brudyi. Albatross Station D5613 (42"00'S, 12lo44'W), South China Sea, 752 fathoms. USNM 12657. la,b-large specimen with crenulated aperture, x29; 2a,b-x42; 3a,b-small specimen displaying streptospiral coiling and oval aperture, x57. Fig. 4a-5b. Cribrustornoides subglubosus forma brudyi. Albatross Station D2035 (39"26'N, 70"02'W), North Atlantic, 1362 fathoms. USNM 10359, 4a,b-x27; 5a,b-x26. Fig. 6a-8b. Cribrostomoides subgloboslrs forma subglobosus. Goldseeker Station in the Faeroe-Shetland Channel (61"03'N, 02"20'W), 1418 m. Cushman Collection (unregistered slide). 6a,b-large specimen with crenulated apertural lips, x46; 7a-8b-small specimens displaying streptospiral coiling, 7a,b-x43; 8a,b-x54. Cushman (sic). He has demonstrated that morphotypes characterised by single interio-areal a p e r t u r e s r e p r e s e n t t h e megalospheric generation a n d t h a t those w i t h multiple areal apertures ("with lips which approach each other in several places even to separate the slit into areal openings") are microspheric a d u l t s (see also o u r Fig. 3). The former have a proloculus diameter of 33p and an overall test diameter of (4) O n the wall structure Both C. subglobosus forma bradyi (Fig.  4) a n d forma subglobosus (PI. 3 ) possess a typically tripartate trochamminacean wall structure with a thick agglutinated layer bounded by inner and Outer Organic layers. The chamber bradyi a n d forma subglobosus are several grains thick with coarse quartz and o t h e r mineral particles in a fineg r a i n e d g r o u n d mass. In C. subglobosus forma bradyi, both the exterior and interior test surfaces are finely agglutinated and smoothly finished, and coarser particles are concentrated within the chamber wall.
In C. subglobosus forma subglobosus, the coarser grains may project outward as well as into the chamber lumen resulting in rough test surfaces. Sectioned, imperforate chamber walls  fig. 4.1 Cribrostomoides sribglobosris forma bradyi. la-Paralectotype sectioned to reveal wall structure x30; lb-Detail of wall, showing the inner organic layer (iol), x510; Ic-wall consists of both biogenic (siliceous) and lithogenic particles with long axes oriented normal to the inner and outer surfaces, (OOL= outer organic layer), x510; Id-Larger particles appear to be concentrated near the centre of the wall, while small particles are placed beneath the IOL and OOL. Undifferentiated organic cement is visible at grain contacts, x510. the line of communication between successive intercameral foramina and the primary aperture.

associated variation in apertural form with alternation of generations in Cribrostomoides bradyi
Of Explanation of Plate 3 W a l l structure of Cribrostomoides subglobosus forma subglobosus. Fig. 1-3 Norwegian-Greenland Sea, Sample 21697-1 (73"45.1'N/10°28.5' W), 3062 m, 1-x40; 2-detail of wall showing inner organic layer (iol), x635; 3-detail of wall showing undifferentiated organic cement at particle contacts, ~3180.  Involute streptospiral Interio-areal ( megalo.)' Cribrostomoides Cushman, 1910Cushrnan, 1910 Saidova, 1981 of well-preserved specimens show an inner organic layer as well as a thin outer organic layer (Fig. 4.lb-d; PI. 3, figs. 2,3, 5-7). In both formae all a g g l u t i n a t e d particles a r e organically enveloped a n d firmly glued together with organic cement. In the distal parts of the chamber wall the cement is developed as morphologically undifferentiated substance which joins particles at their points of contact Fig.  4.ld, P1. 3, figs. 3, 5, 6), while in proximal parts of the wall it may have a net-like appearance (PI. 3, fig. 7). The organic nets are expecially found in contact with the inner organic layer, although they may be incomplete in some chamber wall areas.

DESIGNATION OF LECTOTYPE FOR HAPLOPHRAG-MOIDES SUBGLOBOSUS CUSHMAN, I 9 I 0
The specimen designated as lectotype of Haplophragrnoidcs suhglohosus Cushman, 1910 (United States National Museum of Natural History [USNM] Registered Number USNM8219b) has been chosen from the original syntypic suite of that species. The specimen (Pl. 1, fig. la,b) is from Albatross Station D3603 in the North Pacific (1771fm or 3241m), material from which was certainly available to Cushman at the time he was working on his "Monograph of the Foraminifera of the North Pacific Ocean" (1910). The lectotypification is therefore in accordance with Article 74(a) of the ICZN (Ride ct al., 1985), which states that "If a type series contains more than one specimen and a holotype has not been designated, any author may designate one of the syntypes as a lectotype ... ".
The lectotype is housed in a slide bearing annotations to the effect that it is a "plesiotype" probably representing the specimen figured as Textfig. 164 on p. 106 of the "North Pacific Monograph" (Cushman, 1910) (a plesiotype is a figured specimen used subsequently to t h e original description). The lectotypification is therefore also in accordance with Recommendation 74B of the ICZN, which states that "other things being equal, a n a u t h o r w h o designates a lectotype should give preference to a syntype of which an illustration has been published".
The remaining former s y n t y p e s of H. subglobosus Cushman, 1910 become paralectotypes in accordance with Article 74a(iv) of the ICZN, which states that "The valid designation of a lectotype permanently deprives all specimens that were formerly syntypes ... of the status of syntype [Art. 73b(ii)]; those species become paralectotypes [Rec. 74Fl".

DESIGNATION OF LECJOJYPE FOR CfUBROSJOMOlDES BRADYl CUSHMAN, I 9 I 0
The specimen designated as lectotype of Cribrostornoides bradyi Cushman, 1910 (hitherto unregistered by the USNM) has also been chosen from the original syntypic suite of that species. The specimen ( Fig. 2. la,b) is from Albatross Station D3346 in the North Pacific, material from which was certainly available to Cushman at the time he was working on his "North Pacific Monograph" (Cushman, 1910). The lectotypification is therefore in accordance with Article 74(a) of the ICZN (Ride et al., 1985; see also above). The remaining former syntypes of C. bradyi Cushman, 1910 become paralectotypes in accordance with Article 74a(iv) of the ICZN.

EMENDED DIAGNOSIS OF THE GENUS CfUBROSTOMOIDES
The Foraminifera1 genus Cribrostomoides C Y i hos t o WI o ides C u s h m an, 1 9 1 0, p p s . 1 0 8 1 0 9 [ C . b Y a d y i Cushman, 1910, pps. Hoglund, 19471 .'rest free, coiled in an involute streptospire, characterised by a (repeated) alternation in axis (usually of ninety degrees); wall agglutinated, solid, imperforate, consisting of a multiple layer of mineral particles covered by an inner and outer organic lining, cement organic, aperture equatorial or slightly asymmetricallv placed, interio-areal and single to areal and multiple, surrounded by lips.
The majorit!, of occurrences are either in comparatively shallow (shelf to upper bathyal) depths in high latitudes or comparatively deep (middle bathyiil to abyssal) depths in low to moderate latitudes. The inference is that it is a stenothermal, cryophilic genus. Recent evidence suggests that it might be infaunal in habit (Mackensen & Douglas, 1989).

TAXONOMIC IMPLICATIONS
Our emendation of Cribrostomoirlcs Cushman, 1910 affects the interpretation of its relationship to a number of allied genera Crrbr ostomoidel : Cushman, 1910, as emended heiein, is distingui5hed from Haplophragmozdes Cushman, 1910, emend Hoglund, 1947 and Evolutiiiella Myatlyuk, 1971 on the basis of its streptospiral rather than planispiral coiling and interio-areal rather than interio-marginal aperture, respectively; from Recurvoides Earland, 1934, emend. Uchio, 1960 on the basis of its involute rather t h a n evolute streptospiral coiling and inflated rather than compressed test; from Conglophragmium Bermudez & Rivero, 1963 in its well-formed chambers; from Martyschiella Myatliuk, 1966 andTliulmmanorecurvoides Sandulescu, 1971 on the basis of its involute rather than evolute streptospiral coiling and interio-areal rather than interio-marginal aperture, respectively; from Budashevaeila Loeblich & Tappan, 1964 on the basis of its involute rather than evolute streptospiral coiling, interio-areal rather than interio-marginal aperture a n d inflated rather than compressed test; from Veleroiiinoides Saidova, 1981 on the basis of its involute streptospiral rather than evolute planispiral coiling; from Cribrostomellus Saidova, 1970 on the basis of its organic rather than calcareous cement, and from Buzasinn Loeblich & Tappan (and its synonym Cystamininella Lukina, 1980, iion Myatlyuk, 1966 on the basis of its streptospiral rather than planispiral coiling. Criteria for the discrimination of the aforementioned genera are summarised on Table 1. Lnlwospira Hoglund, 1947 is automatically a synonym of Cribtatornoides Cushman, 1910 because Hoglund included the tvpe species of the latter genus in his description of the former. In our opinion, evolute planispiral species with intcrio-areal apertures previously erroneously included in Lahrospiua Hoglund, 1947 should now be transferred to Vekioiiimides Saidova, 1981. We are currently reviewing the genus Recurvoidella Uchio, 1960 partly in order to elucidate the nature of its relationship with Crihrostomoides Cushman, 1910.