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A review of species names for Ammonia and Elphidium, common foraminifera along the Texas Gulf Coast.

Abstract. -- Species names for Ammonia and Elphidium have continually changed since these taxa were first described in Texas coastal environments. As a result, classification is problematic and the literature is inconsistent. The purpose of this paper is to evaluate the taxonomic status of species currently assigned to Ammonia and Elphidium. This task has been accomplished through extensive literature review and through comparison of specimens from this study with those in the Cushman Collection at the National Museum of Natural History. Most Elphidium found along the Texas coast are assignable to either Elphidium gunteri or E. excavatum, and the Ammonia present are assignable to Ammonia parkinsoniana and A. tepida. Present geographic, molecular and reproductive evidence shows that the species names A. parkinsoniana and A. tepida, not A. beccarii, should be used to describe these morphotypes of Ammonia wherever they occur, including the Gulf of Mexico, the east coast of North America, the Caribbean and the Pacific.

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Since recent foraminifera on the Texas Gulf Coast were first described (Kornfeld 1931; Phleger & Parker 1951; Post 1951; Parker et al. 1953), species names for the most common estuarine taxa, Ammonia and Elphidium, have continually changed in the literature, making it difficult for subsequent workers to identify specimens. Specific names of these foraminifera have changed as it was recognized that many of the Gulf Coast morphotypes (shell types) are also found around the world (Miller et al. 1982; Buzas et al. 1985; Walton & Sloan 1990; Hayward et al. 1997; 1999), and that rather than being many separate species, a single species can have a variety of morphotypes (Schnitker 1974; Poag 1978; Miller et al. 1982; Walton & Sloan 1990; Stouff et al. 1999a).

The purpose of this paper is to assess the species names for the most commonly encountered morphotypes of Ammonia and Elphidium found in Texas coastal environments. The taxonomy proposed for Ammonia herein also affects the species name used for this morphotype on a worldwide basis. To determine current taxonomy, a survey of the literature was undertaken and specimens from Laguna Madre, Nueces Bay, the Arroyo Colorado, and Laguna Atascosa were compared with specimens in the Smithsonian National Museum of Natural History.

[FIGURE 1 OMITTED]

METHODS

Sediment cores, varying from 33 cm to 95 cm in length depending on bottom conditions, were taken at four sites along the south Texas coast: Nueces Bay, southern Laguna Madre, the Arroyo Colorado, and Laguna Atascosa (Fig. 1). Since the spatial distribution of foraminifera is not uniform (Buzas 1968), four cores were taken at each locality in order to get an accurate representation of the taxonomic assemblages.

To evaluate living foraminifera present during sampling, the top 2 cm of the cores was stained with rose Bengal (Walton 1952; Murray & Bowser 2000), a protein-specific stain. Cores were sliced in 1 to 5 cm intervals (depending on other analyses performed), and 20 ml of sediment from selected intervals was washed through a 230 mesh (.062 mm) sieve. If foraminifera were not abundant, as in the Arroyo Colorado samples, they were concentrated for ease of counting using a sodium polytungstate flotation technique (Callahan 1987). From each locality, approximately 300 foraminifera were counted from the surface sediments of each core and from different depths in at least one core per site.

Specimens of Elphidium gunteri, E. excavatum, Ammonia parkinsoniana and A. tepida figured herein have been deposited in the Cushman Collection, National Museum of Natural History (USNM).

RESULTS

Elphidium gunteri, E. excavatum, Ammonia parkinsoniana and A. tepida (Figure 2) are the most common taxa at the sampling localities, together comprising from 60% to over 90% of the total assemblage in surface sediments and at depth. A range of shell types is exhibited within each of these species. Other taxa present at the sites are Quinqueloculina seminula, Haynesina germanica and Ammotium salsum (for a complete account of taxa, see Buzas-Stephens 2001).

Living Ammonia and Elphidium were found at all localities except for the Arroyo Colorado, where there were no living Ammonia and overall numbers (living plus dead) of Ammonia are low. The river has a history of poor water quality conditions (Bryan 1971) that may be responsible for the paucity of Ammonia (Buzas-Stephens 2001).

Interestingly, perfectly preserved Cretaceous through Eocene age foraminifera are present in the samples from southern Laguna Madre, the Arroyo Colorado, and Laguna Atascosa. Since much of the sediment in southern Laguna Madre is derived from offshore, many of these specimens are probably reworked at least a couple times from old Rio Grande delta distributary deposits (Rusnak 1960).

SYSTEMATICS

Identification of the different species of Ammonia and Elphidium was accomplished through comparison of specimens from this study with those housed in the Cushman Collection, National Museum of Natural History (NMNH) in Washington, D.C. To ascertain identifications, hypotypes and specimens from Phleger & Parker (1951), Parker et al. (1953) and Poag (1981) were examined. Although many other authors have recorded species of Ammonia and Elphidium in Texas coastal environments (for a compilation, see Culver & Buzas 1981), most of these taxa are not illustrated and thus not available for comparison in future studies such as this.

Preliminary attempts to classify specimens from this work through illustrations and micrographs from Phleger & Parker (1951), Parker et al. (1953) and Poag (1981) were largely unsuccessful. Correct identifications were made only through direct comparison of individuals under the light microscope. Unless a worker is thoroughly familiar with an assemblage, identifications should be based on actual specimens, and not on figures from the literature.

The following taxonomy through the genus level is from Loeblich & Tappan (1987). Synonymies are presented for foraminiferal studies specific to the Texas Gulf Coast. Micrographs were taken with a Philips XL 30 ESEM.
Figure 2a
 Order FORAMINIFERIDA Eichwald
 Suborder ROTALIINA Delage & Herouard
 Superfamily ROTALIACEA Ehrenberg
 Family ELPHIDIIDAE Galloway
 Subfamily ELPHIDIINAE Galloway
 Genus Elphidium de Montfort
 Elphidium gunteri Cole


Elphidium gunteri Cole, 1931:34, pl. 4, figs. 9, 10.--Parker et al., 1953:8, pl. 3, figs. 18-19.--Parker, 1954:508, pl. 6, fig. 16.

Elphidium gunteri Cole var. galvestonensis.--Kornfeld (part), 1931:87-88, pl. 15, figs. 2a, b, 3a, b (not figs. 1a, b).--Post, 1951:172, pl. 1, fig. 14.

Elphidium gunteri Cole var. galvestonense--Phleger & Parker, 1951:10, pl. 5, figs. 13-14.

Cellanthus gunteri Cole, Wantland, 1969:109, pl. 3, fig. 5.

Elphidium gunteri forma typicum--Poag, 1978:402, pl. 2, figs. 13-16, 22-23.--Poag, 1981:61-62, pls. 37-38, figs. 1a, b.

Material examined.--USNM 517707.

Distribution. -- Elphidium gunteri comprises 8% of the total taxa in the surface sediments (0-2 cm) of Nueces Bay, 17% in Laguna Madre, 80% in the Arroyo Colorado and 10% in Laguna Atascosa.

Remarks. -- As in coastal environments worldwide (Miller et al. 1982; Hayward 1997), the wide range of Elphidium shell types present along the Texas Gulf Coast provides a continual challenge to researchers attempting to assign them to species. One of the most common estuarine forms, which has straight sutures, prominent sutural bridges and umbilical bosses, and large, widely spaced pores has been consistently assigned to Elphidium gunteri Cole (Kornfeld 1931; Phleger & Parker 1951; Post 1951; Parker et al. 1953; Wantland 1969; Poag 1978; 1981) (Figure 2a). However, the above characteristics defining E. gunteri grade into other common morphotypes, including E. excavatum (Terquem) (Figures 2b & c). Since the characteristics of E. gunteri and E. excavatum can overlap (Buzas et al. 1985), it is sometimes difficult to assign a specimen to a species, even after counting thousands.
Figures 2b & c
 Elphidium excavatum (Terquem)


Polystomella excavata Terquem, 1875:25, pl. 2, fig.2.

Elphidium translucens (Natland).--Post, 1951:173, pl. 1, fig. 17.--Parker et al, 1953:9, pl. 3, fig. 27.

Protelphidium delicatulum (Bermudez).--Wantland, 1969:110, pl. 3, fig. 7.

Elphidium delicatulum (Bermudez).--Parker et al., 1953:7, pl. 3, figs. 12, 17. Elphidium gunteri Cole forma salsum.--Poag, 1978:402, pl. 2, figs. 1-12, 17-21.--Poag, 1981:61, pls. 37-38, figs. 2, 2a, b.

Material examined.--USNM 517708, 517709.

Distribution. -- In the surface sediments Elphidium excavatum makes up 15% of the assemblage in Nueces Bay, 17% in Laguna Madre, 8% in the Arroyo Colorado and 11% in Laguna Atascosa.

Remarks. -- Also ubiquitous to coastal environments worldwide (Miller et al. 1982; Buzas et al. 1985; Hayward 1997), Elphidium excavatum can generally be distinguished from E. gunteri by the presence of more numerous and smaller pores, lesser development of sutural bridges and fewer umbilical bosses. Because these features can vary widely within the species, E. excavatum has "probably been misidentified more than any other foraminiferal species" (Buzas et al. 1985). Until this study, the name E. excavatum has never been assigned to Texas coastal Elphidium, though Culver & Buzas (1981) provided synonymies in their compilation of foraminiferal studies from the Gulf of Mexico. Instead, E. excavatum has mostly been referred to as E. translucens (Post 1951; Parker et al. 1953) or E. delicatulum (Parker et al. 1953; Wantland 1969), though it surely has had other synonyms as well. In the current project, E. excavatum and E. gunteri together comprise about 98% of all Elphidium found at each site, making these two species the most widespread and abundant species of Elphidium in southern Texas estuaries.

Although some authors have correlated the different shell types of E. gunteri and E. excavatum with environmental variables (Poag 1978; Miller et al. 1982), a similar correlation cannot be seen in this study. Perhaps future DNA and/or reproductive studies will help clarify the extent of genetic versus environmental control over the production of different Elphidium shell types.
Figures 2f & g
 Family ROTALIIDAE Ehrenberg
 Subfamily AMMONIINAE Saidova
 Genus Ammonia Brunnich
 Ammonia parkinsoniana (d'Orbigny)


Rosalina parkinsoniana d'Orbigny, 1839:99, pl. 4, figs. 25-27.

Rotalia beccarii (Linne' var. parkinsoniana (d'Orbigny).--Kornfeld, 1931:90-91, pl. 13, figs. 1a, b, c.--Phleger & Parker, 1951:23, pl. 12, figs. 6a, b.

Rotalia beccarii (Linne').--Post, 1951:176, pl. 1, fig. 20.

Rotalia beccarii (Linne') variant A.--Parker et al., 1953:13, pl. 4, figs.20-22.

Rotalia beccarii (Linne') variants.--Parker, 1954:531, pl. 10, figs. 1, 2, 5, 6.

Ammonia beccarii (Linne') variants.--Wantland, 1969:109, pl. 3, figs. 1a, b, c.

Ammonia parkinsoniana (d'Orbigny) forma typica.--Poag, 1978:397, pl. 1, figs. 5-9, 13-16, 19-21.--Poag, 1981:38, pls. 45-46, figs. 1, 1a, 1b.

Material examined.--USNM 517710, 517711.

Distribution. -- In surface sediments, Ammonia parkinsoniana comprises 63% of the total fauna in Nueces Bay, 21% in Laguna Madre, 4% in the Arroyo Colorado and 32% in Laguna Atascosa.

Remarks. -- Among the different species of Ammonia found worldwide, there are three very common forms (Walton & Sloan 1990): (1) An ornamented shell morphotype that has distinct beading, fluting and/or furrowing along the sutures on one or both sides, and an umbilical plug (Figures 2d, e). This form was first described from the Mediterranean as A. beccarii (Linne' 1758); (2) An unornamented morphotype with an umbilical plug that lacks the above beading/fluting/furrowing along sutures (Figures 2f, g). This form was first described from the Caribbean as A. parkinsoniana (d'Orbigny 1839); and (3) A smaller, more lobate morphotype that has neither ornamentation nor an umbilical plug (Figures 2h, i), also first described from the Caribbean. This third morphotype is probably the A. catesbyana of d'Orbigny (1839). When updating d'Orbigny's Cuban collection, Le Calvez (1977) designated a neotype for A. parkinsoniana, but apparently no identifiable specimens of A. catesbyana were available for the designation of a neotype for this species. In addition, d'Orbigny's type figures are vague (Poag 1978), leaving the formal species name for the small lobate morphotype in question.

As well as having differences in overall appearance, the three morphotypes vary in their geographic ranges. The ornamented form occurs mainly in northern waters such as the Mediterranean, the northeastern Atlantic (no references are available south of 27N in the eastern Atlantic), and the western Atlantic near Cape Cod (Walton & Sloan 1990). The other two morphotypes are found around the world (Walton & Sloan 1990), and are exclusive to southern oceans including the Pacific, Indian, and south Atlantic (Walton & Sloan 1990). They also occur in Texas estuaries and near shore in the Gulf of Mexico (Poag 1981; Walton & Sloan 1990).

In the early 1900s, Cushman (1926) began using the species name A. beccarii for all three forms, using variety names to distinguish them, and this terminology persisted. Thus the ornamented form was called A. beccarii var. beccarii, the one without ornamentation was A. beccarii var. parkinsoniana, and the lobate one without a plug was A. beccarii var. tepida. Many workers today refer to the smaller, lobate form as A. tepida, the varietal name first used by Cushman (1926). Neither "variety" nor "forma" names is governed by the International Code of Zoological Nomenclature (Ride et al. 1985).

In their classic studies documenting Texas Gulf Coast foraminifera, Kornfeld (1931), Phleger & Parker (1951) and Parker et al. (1953) also used the names A. beccarii var. parkinsoniana and A. beccarii var. tepida (or "Rotalia" beccarii, as the generic name became for awhile). Poag (1978) reinstated d'Orbigny's original name, Ammonia parkinsoniana, for the unornamented shell type, designating it as A. parkinsoniana forma typica. He called the lobate form Ammonia parkinsoniana forma tepida. Poag (1978) asserted that A. parkinsoniana was a different species than A. beccarii because the ornamented form does not occur in southern oceans (Poag 1978; Walton & Sloan 1990). Since Poag's re-introduction of the name A. parkinsoniana, both A. parkinsoniana (see Yuill 1991; Colburn & Baskin 1998) and A. beccarii (see Williams 1995) have been used to describe Texas Gulf Coast Ammonia.

More recent investigations into the DNA (Pawlowski et al. 1995; Holzmann & Pawlowski 1997; Holzmann 2000) and the life cycle (Goldstein & Moodley 1993; Stouff et al. 1999a) of Ammonia are helping to clarify the role genetics plays in producing these shell types. Through ribosomal DNA sequencing, Pawlowski et al. (1995) determined that the three morphotypes have distinct sequences indicating that they are separate species. Another molecular study (Holzmann & Pawlowski 1997) again shows that A. tepida can be distinguished genetically from another Ammonia morphotype. Holzmann (2000) further shows how different species of Ammonia found worldwide can be characterized according to morphology and DNA.

In the most current reproductive study, Stouff et al. (1999a) found that the different stages in the life cycle of Ammonia tepida have a characteristic shell forms. The asexual, diploid schizont stage typically has one or more umbilical plugs, while the sexual, haploid gamont stage lacks an umbilical plug. They did not observe the ornamented form as part of the life cycle of A. tepida or as a result of ontogeny. Likewise, ornamented offspring have not been produced from any cultures of A. tepida to date (Bradshaw 1957; Schnitker 1974; Goldstein & Moodley 1993; Stouff et al. 1999). However, Schnitker (1974) cultured two individuals of the ornamented form (A. beccarii), and reported "most of their offspring were similar to the tepida offspring".

To summarize, present geographic, reproductive, and molecular evidence show that the ornamented, unornamented and lobate morphotypes of Ammonia are separate species. Since the name A. beccarii was first assigned to the ornamented morphotype (Linne' 1758), it should be reserved exclusively for this form. The name A. parkinsoniana (d'Orbigny 1839) is the valid name for the unornamented form, and apparently other authors agree with this conclusion (Jorissen 1988; Sen Gupta et al. 1996; Colburn & Baskin 1998; Hayward et al. 1999).
Figures 2h & i
 Ammonia tepida (Cushman)


Rotalia beccarii (Linne') var. tepida Cushman, 1926:79, pl. 1.--Kornfeld, 1931:91, pl. 13, figs. 3a, b, c.--Phleger & Parker, 1951:23, pl. 12, figs. 7a, b.--Post, 1951:176, pl. 1, figs. 21, 22.

Rotalia beccarii (Linne') variants B, C.--Parker et al., 1953:13, pl. 4, figs. 25-30.

Rotalia pauciloculata (Phleger & Parker).--Phleger & Parker, 1951:23, pl. 12, figs. 8a, b, 9a, b.--Parker et al., 1953:13-14, pl. 4, figs. 31, 37.

Ammonia pauciloculata (Phleger & Parker).--Poag, 1981:38-39, pls. 45-46, figs. 3, 3a, b.

Ammonia beccarii (Linne') variants.--Wantland, 1969:109, pl. 3, figs. 2a, b, c, 3a, b, c.

Ammonia parkinsoniana (d'Orbigny) forma tepida.--Poag, 1978:397, pl. 1, figs. 1-4, 10-12, 17, 18.--Poag, 1981:37-38, pls. 45-46, figs. 2, 2a, b.

Material examined.--USNM 517712, 517713.

Distribution. -- Ammonia tepida comprises 2% of the assemblage in the surface sediments of Nueces Bay, 4% in Laguna Madre, 4% in the Arroyo Colorado and 39% in Laguna Atascosa. Ammonia tepida is more abundant than A. parkinsoniana at the sites with lower salinities (the Arroyo Colorado and Laguna Atascosa) (Table 1). Hayward et al. (1999) note a similar correlation with salinity, but Poag (1978) observed the opposite.

Remarks. -- Although the taxonomy for the small, lobate morphotype will not be stabilized until a neotype is established, it is recommended that this form be assigned to Ammonia tepida since this name is already widely used (Pawlowski et al. 1995; Yanko et al. 1994; 1998; Geslin et al. 1998; Stouff et al. 1999a; 1999b).

CONCLUSIONS

The most common estuarine foraminifera found along the Texas Gulf Coast are Elphidium gunteri, E. excavatum, Ammonia parkinsoniana and A. tepida. These species are also found worldwide. Since the defining characteristics of E. gunteri and E. excavatum overlap, care must be exercised when assigning species names to these forms. Elphidium excavatum, in particular, exhibits a wide range of shell morphotypes and thus can be quite challenging to identify. Current geographic, molecular and reproductive evidence shows that A. parkinsoniana and A. tepida have erroneously been called A. beccarii for most of the 20th century. The unornamented morphotype of Ammonia should be called A. parkinsoniana and the small, lobate form is A. tepida.
Table 1. Percent of Ammonia parkinsoniana versus Ammonia tepida as
compared to salinity.

 Nueces Laguna Arroyo Laguna
 Bay Madre Colorado Atascosa

Salinity 27 ppt 26 ppt 14 ppt 6 ppt

A. Parkinsoniana 96% 82% 45% 45%
A. tepida 4% 18% 55% 55%


ACKNOWLEDGMENTS

This research was partially funded by Geological Society of America grant 6148-97. The authors also wish to thank Martin A. Buzas for kindly reviewing the manuscript.

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Pamela Buzas-Stephens, Emile A. Pessagno, Jr. * and C. Jerry Bowen

Department of Biology, Midwestern State University 3410 Taft Blvd., Wichita Falls, Texas 76308 and * Department of Geosciences, University of Texas at Dallas P.O. Box 830688, Richardson, Texas 75083

PB-S at: pamela.stephens@mwsu.edu
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Author:Buzas-Stephens, Pamela; Pessagno, Emile A., Jr.; Bowen, C. Jerry
Publication:The Texas Journal of Science
Geographic Code:1U7TX
Date:Feb 1, 2002
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