A survey of the testate amoeba genus Difflugia Leclerc, 1815 based on specimens in the E. Penard and C. G. Ogden collections of the Natural History Museum, London.
Part 2: species with shells that are pyriform or elongate

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Protistology 8 (4), 133−171 (2014)
Protistology
A survey of the testate amoeba genus Difflugia Leclerc, 1815 based on specimens in the E. Penard and C.G. Ogden collections of the Natural History Museum, London. Part 2: Species with shells that are pyriform or elongate
Yuri Mazei1 and Alan Warren2
1 Department of Zoology and Ecology, Penza State University, Penza, Russia
2 Department of Life Sciences, Natural History Museum, London, UK
Summary
We review the species of Difflugia with a shell that is pyriform or elongate, based primarily on examinations of two collections in the Natural History Museum, London, UK: (i) Penard’s collection of balsam-mounted microscope slides, and (ii) Ogden’s scanning electron micrographs and shell measurements. We discuss taxa grouped into seven species complexes, namely Difflugia oblonga Ehrenberg, 1838, Difflugia pyriformis Perty, 1849, Difflugia bryophila (Penard, 1902) Jung, 1942, Difflugia linearis (Penard, 1890) Gautier-Lievre et Thomas, 1958, Difflugia gigantea (Chardez, 1967) Ogden et Fairman, 1979, Difflugiapetricola Cash, 1909, and Difflugia lanceolata Penard, 1890.
Within the D. oblonga-complex we: (i) distinguish as a separate taxon the typical form of D. oblonga Ehrenberg, 1838- (ii) synonymise D. parva (Thomas, 1954) Ogden, 1983, D. lacustris (Penard, 1899) Ogden, 1983, D. bacillifera Penard, 1890, D. oblonga var. incondita Gauthier-Lievre et Thomas, 1958, and D. oblonga f. cyphodera Jung, 1942 with D. oblonga. Within the D. pyriformis-complex we: (i) distinguish as separate taxa the typical form of D. pyriformis Perty, 1849, as well as D. capreolata Penard, 1902, and (ii) synonymise D. cylindrus (Thomas, 1953) Ogden, 1983 with D. pyriformis Perty, 1849. Within the D. bryophila-complex we: (i) distinguish as a separate taxon D. bryophila (Penard, 1902) Jung, 1942, and (ii) synonymise D. gassowskii (Gassowsky, 1936) Ogden, 1983 with D. bryophila. Within the D. linearis-complex we: (i) distinguish as a separate taxon D. linearis (Penard, 1890) Gautier-Lievre et Thomas, 1958, and (ii) synonymise D. paulii Ogden, 1983 and D. nebelondes Gauthier-Lievre and Thomas, 1958 with D. linearis. Within the
D. gigantea-complex we: (i) distinguish as a separate taxon the typical form of D. gigantea (Chardez, 1967) Ogden et Fairman, 1979, and (ii) discuss the validity of D. oblonga var. angusticollis Stepanek, 1952, and D. oblonga var. stepaneki (Stepanek, 1952) Decloitre. Within the D. petricola-complex we accept D. petricola Cash, 1909 as a valid species and suggest its possible relationships with other Difflugia species.
© 2014 The Author (s)
Protistology © 2014 Protozoological Society Affiliated with RAS
134 • Yuri Mazei and Alan Warren
Within the D. lanceolata-complex we accept D. lanceolata Penard, 1890 as a valid species and illustrate its variability based on C.G. Ogden’s SEM micrographs.
As in the first part of this series of papers in which we taxonomically revise the genus Difflugia we conclude that, based on current knowledge, it is unclear whether these species complexes represent single, highly polymorphic species, or groups of sibling species. Further studies based on a combination of morphometric, ultrastructural (SEM), molecular, and environmental data are needed in order to characterize these species complexes in more detail and thus resolve their systematics.
Key words: Difflugia, morphospecies, species complex, taxonomic revision, testate amoebae
Introduction
This is the second of a series of papers that aims to review the genus Difflugia based primarily on examinations of two collections in the Natural History Museum (NHM), London, UK, i.e. Penard’s collection of balsam-mounted microscope slides, and Ogden’s scanning electron micrographs (SEM) and shell measurements, and also on published literature. In the first paper of this series (Mazei and Warren, 2012) we reviewed those species of Difflugia with a shell that is pointed aborally and/ or has aboral protuberances. The aim of the present paper is to review those species with a shell that is pyriform or elongate.
Review of the literature on the taxonomy of selected Difflugia species.
Leclerc (1815) erected the genus Difflugia, however he failed to use binary nomenclature and did not give specific names to any of the organisms he described (Fig. 1). A year later Lamarc (1816, p. 95) attributed the name D. proteiformis to the forms described by Leclerc in 1815 but did not provide any descriptions discriminating between them. Later Ehrenberg (1838a, p. 131- 1838b, table 9, fig.
1) applied the name D. proteiformis to those forms which «appear rather to apply to the D. globulosa of Dujardin» (Leidy, 1879, p. 105). Dujardin (1841, p. 248−249) distinguished both D. globulosa and D. proteiformis noting that although both species are globular to ovoid in shape, the former is 100−250 pm long and has a smooth surface whereas the latter has a length of 45−112 pm and is covered by sand grains. Dujardin did not illustrated the latter species. Perty (1852) applied name D. proteiformis to those specimens of Lecrec shown on his plate 17, fig. 1 (Fig. 1) which are currently known as Lesquereusia modesta (Cash and Hopkinson, 1909). Thus, as
noted by Ogden and Ellison (1988), the taxonomy of Difflugia proteiformis remains questionable.
Among the specimens of Difflugia figured by Leclerc (1815- Fig. 1) two are currently recognized as valid: D. pyriformis (figs 2- 3 of Fig. 1) and D. acuminata (fig. 5 of Fig. 1). Leidy (1879, p. 98) and Penard (1902, p. 214), for example, both treated Leclerc’s figs 2 and 3 as D. pyriformis.
Ehrenberg (1831, p. 90) listed three species of Difflugia, namely D. proteiformis Leclerc, D. oblonga Ehrenberg, and D. acuminata Ehrenberg, with a briefdescription of each. Later Ehrenberg (1838a, 1838b) described Difflugia oblonga in more detail as having a shell that is ovoid-elongate, laterally circular, with a smooth surface, generally transparent in appearance, and 110 pm long (Fig. 2).
Perty (1849, 1852) described Difflugia pyriformis (Fig. 3, a-c) the shell of which is 140−200 pm long, pyriform or sometimes irregular in shape, and with a rough surface (Fig. 3c). He also questioned the validity of D. oblonga (Fig. 3d) noting that he had found specimens of D. pyriformis that were similar shape to D. oblonga and had a surface structure that was similar to D. proteiformis, which he considered should be Lesquereusia molesta (Perty, 1852).
Wallich (1864) provided first hypothetical scheme showing relationships between different testate amoebae including notes on D. oblonga and
D. pyriformis (Fig. 4). He mentioned «…four so-called species, namely, D. proteiformis, D. oblonga,
D. acuminata (Ehr.), and D. pyriformis (Perty)» (Wallich, 1864, p. 222). He described D. oblonga as having an almost cylindrical shape (fig. 3t on his plate XV — Fig. 4a) and characterized D. pyriformis by its clearly pyriform shape (fig 3s on his plate XV — Fig. 4a- figs 9- 10 on his plate XVI — Fig. 4b). However, in his systematic scheme (p. 240) he recognized only one valid species within the genus Difflugia, namely D. proteiformis (Ehrenberg) with four subspecies. One of these subspecies, i.e. D.
Protistology ¦ 135
mitriformis (Wall.), consisted of four varieties: D. acuminata (Ehr.), D. spiralis (Leclerc), D. pyriformis (Perty), and D. lageniformis (Wall.). He described the shell of D. pyriformis as «varying from the pear- to the ballon-shape» (Wallich, 1864, p. 240). This means that according to Wallich (1864), D. oblonga is a variety of D. pyriformis. Carter (1864) also used the name D. pyriformis and, according to his illustrations, included forms with shells that are elongate, pyriform, or acuminate (Fig. 5).
Leidy (1879) described Difflugia pyriformis as varying considerably in size and shape and distinguished following varieties within this species: 'pyriformis', 'compressa', 'nodosa', 'cornuta', and 'vas'. Even the typical D. pyriformis appeared to be highly polymorphic (Fig. 6). Regarding D. oblonga Leidy (1879, p. 105) argued that «…in its shape it appears rather to be related with D. acuminata without its point» and thus did not consider D. oblonga and D. pyriformis as synonyms.
Penard (1890) followed Leidy’s approach, recognizing within D. pyriformis the varieties 'nodosa' and 'vas' and describing the new taxa D. pyriformis var. linearis and D. pyriformis var. tenuis (Fig. 7). Later he added the varieties D. pyriformis var. lacustris (Penard, 1899) and D. pyriformis var. bryophila (Penard, 1902) and described three new species that are closely related to D. pyriformis, namely D. lanceolata, D. bacillifera (Penard, 1890), and D. capreolata (Penard, 1902). It is noteworthy that Penard (1890, p. 145- 1902, p. 250) considered
D. lanceolata as closely related with D. acuminata,
i.e. in terms of size and general appearance and the lack of an acuminated end of the shell. Given the similarity of D. lanceolata sensu Penard and D. oblonga sensu Ehrenberg (compare Fig. 2d and Fig. 7q, t, u, v), it is evident that Penard followed the principle established by Leidy (1879).
Cash and Hopkinson (1909) and Cash et al. (1919) revived the concept of Difflugia oblonga. They argued that «although this species is now almost universally called Difflugia pyriformis, Ehrenberg’s name has the priority and must be adopted in accordance with the rule of zoological nomenclature» (Cash and Hopkinson, 1909, p.
8). Subsequently they listed some of the known taxa, such as typical D. oblonga (Fig. 8, a-c, f-g), D. oblonga var. lacustris (Fig. 8, d-e), D. oblonga var. bryophila (Fig. 8o), D. lanceolata (Fig. 8, k-m), and
D. bacillifera (Fig. 8n), and described the new species
D. petricola (Fig. 8, h-j). It is interesting that Wailes and Penard (1911) used the name D. oblonga var. bryophila despite the fact that Penard (1902) had previously referred to it as D. pyriformis var. bryophila. Jung (1942) subsequently raised this taxon to
Fig. 1. Plate illustrating the first described Difflugia
(Leclerc, 1815, plate 17).
species rank as D. bryophila. Four additional varieties were established during the following decades:
D. oblonga var. longicollis (Gassowsky, 1936), D. oblonga var. cylindrus (Thomas, 1953), D. oblonga var. elongata (van Oye, 1953), and D. oblonga var. parva (Thomas, 1954).
Stepanek (1952) proposed hypothetical schemes describing morphological relationships between pyriform and acuminate species of Difflugia. Stepanek’s entire scheme is reproduced in our previous publication (Mazei and Warren, 2012) — here we present a reduced version, which is important for discussing taxa with pyriform and elongate shells (Fig. 9). In his exhaustive study of Difflugia in a single pond, Stepanek (1952) recorded numerous transitional forms within the D. oblonga 'ultraspecies' and in many cases made decisions concerning synonymy. For example, he noted that «the surface of the test is covered according to the material provided by the environment and also according to
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Fig. 2. Description of Difflugia oblonga from Ehrenberg’s book (Ehrenberg, 1838a) and atlas (Ehrenberg, 1838b). a — front page of the book- b — front page of the atlas- c — description of D. oblonga (Ehrenberg, 1838a, p. 131) — d — illustration of D. oblonga (Ehrenberg, 1838b, table 9, fig. 2).
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Fig. 3. Difflugiapyriformis and D. oblonga from Perty (1852). a — front page of the book (Perty, 1852) — b — illustration of D. pyriformis (table 9, fig. 9) — c — description of D. pyriformis (p. 187) — d — description of D. oblonga (p. 187).
the quantity present in the environment» (Stepanek, 1952- p. 22). He found a continuum offorms between those species with shells covered by sand grains and those covered by diatom frustules, concluding that coverage by diatoms cannot be regarded as a good feature for species (or even sub-species or variety) separation. Consequently, he synonymised D. bacilliferawith D. oblonga. Similarly he synonymized
D. oblonga var. lacustris with D. oblonga noting that: «In some cases I observed fission of this [Difflugia oblonga var. lacustris] species. It is interesting that on a new specimen the building material settles in most
cases first at the aperture, and in case of a scarcity of material in shards do not cover the remaining surface of the test at all, or they cover it only very scantily» (Stepanek, 1952- p. 22). But such uneven distribution of xenosomes is one of the accepted diagnostic features of D. oblonga var. lacustris. Stepanek also concluded that D. oblonga f. cyphodera described by Jung (1942) and D. pyriformis var. bryophila described by Penard (1902) should be synonymized with D. oblonga. Nevertheless, he erected two new varieties, namely D. oblonga var. angusticollis and
D. oblonga var. vas. Finally, he suggested lumping
138 • Yuri Mazei and Alan Warren

«СЩШ. Ыакк knatrafa. W
Fig. 4. Difflugiapyriformisand D. oblonga from Wallich (1864). a — plate XV of Wallich’s paper showing.. the order in which the four subspecies of Difflugia proteiformis arrange themselves around a common archetypal … centre.» (Wallich, 1864, p. 243) — b — illustration of D. pyriformis from plate XVI ofWallich’s paper showing on fig. 9 «. how completely the test is made up of frustules and valves of diatoms.» and on fig. 10 «common form … [with] moderately large sandy granules» (Wallich, 1864, p. 244).
D. lanceolata with D. oblonga based primarily on the resemblance of the former with the first description of D. oblonga made by Ehrenberg (1838a, 1838b).
In their report on the testate amoebae of Africa, Gauthier-Lievre and Thomas (1958) grouped the various Difflugia spp. based on shell morphology. The following known species were included in the groups entitled «Allongees», and (in part) «Pyriformes», i.e. those with shells that are elongated or pyriform, respectively: D. lanceolata Penard, 1890, D. oblonga var. cylindrus Thomas, 1953, D. oblonga var. elongata van Oye, 1953, D. bacillifera Penard, 1890, D. bryophila (Penard, 1902) Jung,
1942, D. capreolata Penard, 1902, D. oblonga Ehrenberg, 1838 (note that Gauthier-Lievre and Thomas treated D. pyriformis as a synonym of D. oblonga), D. oblonga var. parva Thomas, 1954, D. oblonga var. lacustris Penard, 1902, and D. oblonga var. longicollis Gassowsky, 1936. Furthermore, they raised D. oblonga (pyriformis) var. linearis Penard, 1890 to species rank as D. linearis and described two new taxa from Africa: D. nebelol'-des and D. oblonga var. incondita (Gauthier-Lievre and Thomas, 1958).
Following a review of the diagnostic features of Difflugia oblonga, Chardez (1967) recognized 12 infraspecific forms excluding those with shells
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Fig. 5. Difflugia pyriformis from Carter (1864). a — typical form- b — acuminate variety of the test- c — pyriform variety.
that are neither elongate nor pyriform (Fig. 10): D. oblonga Ehrenberg, 1838 (note that Chardez (1967) treated D. pyriformis as a synonym of D. oblonga), D. oblonga var. gigantea Chardez, 1967 (this taxon was erected by Chardez (1967) based on some illustrations from Leidy, 1879), D. oblonga var. lacustris Penard, 1902, D. oblonga var. cylindrus Thomas, 1953, D. oblonga var. elongata van Oye, 1953, D. oblonga var. parva Thomas, 1954, D. oblonga var. incondita Gauthier-Lievre and Thomas, 1958, D. oblonga f. cyphodera Jung, 1942, D. oblonga var. angusticollis Stepanek, 1952 (note that Chardez (1967) used the name 'angusticaulis', however in the original description by Stepanek (1952) it is 'angusticollis'), D. oblonga var. stepaneki (Stepanek, 1952) Decloitre (known previously as D. oblonga var. vas Stepanek, 1952), D. oblonga var. longicollis Gassowsky, 1936, and D. oblonga var. rocki Stepa-nek, 1963).
Subsequently, Chardez and Decloitre (1973) concluded that Difflugia oblonga Ehrenberg, 1838 and Difflugia pyriformis Perty, 1849 are distinct species. Although both have a great range in size (length 80−300 qm in D. oblonga and 90−400 qm in
D. pyriformis), D. oblonga could be separated from
D. pyriformis by its elongate-ovoid shell with smooth surface and its more conspicous neck, however it did not correspond with the figures they provided. They also supplied a list of varieties and forms attributed to D. pyriformis which was identical to those listed by Chardez (1967).
In a series of publications C.G. Ogden redescribed, and in many cases changed the taxonomic status, of 14 taxa of Difflugia with pyriform or elongate shells: D. oblonga, D. pyriformis, D. gigantea, D. bacillifera, D. lacustris, D. bryophila,
D. capreolata, D. lanceolata, D. parva, D. paulii, D. petricola, D. gassowskii, D. linearis, and D. cylindrus (Ogden, 1980, 1983, 1984- Ogden and Fairman, 1979- Ogden and Hedley, 1980- Ogden and Zivko-vic, 1983). Unfortunately, a direct comparison of all of the species listed above was never made in a single publication. It is noteworthy that Ogden (1980) supported the suggestion of Chardez and Decloitre (1973) and clearly distinguished D. oblonga from D. pyriformis based on morphometric and SEM data. We discuss this in more detail below.
We have applied Ogden’s morphometric data (both published and unpublished) to compare the 14 species mentioned above, 11 of which are morphologically similar, the other three (D. gigantea, D. capreolata, and D. lanceolata) being easily distinguished by their size and/or other morphological features (Fig. 11). Scanning electron micrographs of each of these 14 species are reproduced here to the same scale in order to faciliate comparisons of both size and external morphology of 'typical' individuals (Fig. 12).
According to the scatter plot (Fig. 11) we can distinguish five main size classes: (1) large and broad with a shell length of 150−265 qm and shell width 95−145 qm, comprising D. pyriformis, D. cylindrus, and D. capreolata (not shown in the figure), and some individuals identified by C. Ogden as D. oblonga- (2) relatively large and narrow, with a shell length of 130−230 qm and shell width 55−95 qm, comprising D. oblonga, D. lacustris, D. parva, and
D. bacillifera- (3) medium-size and broad, with a shell length of 100−150 qm and shell width 60−100 qm, comprising D. petricola- (4) relatively small and broad, with a shell length of 90−130 qm and shell width 45−70 qm, comprising D. bryophila and
D. gassowskii- (5) small and narrow, with a shell length of 85−120 qm and shell width 30−45 qm, comprising D. linearis and D. paulii. Thus, according to these size classes we can distinguish five species complexes (sensu Foissner and Korganova, 2000):
D. pyriformis-complex, D. oblonga-complex, D.
140 • Yuri Mazei and Alan Warren
Fig. 6. Difflugia pyriformis from Leidy (1879).
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Fig. 7. Difflugia pyriformis and related species from Penard (1890, 1899, 1902). a-c — typical form of D. pyriformis (Penard, 1890, plate III, figs 30, 31, 33) — d — D. pyriformis var. linearis (Penard, 1890, plate III, fig. 42) — e — D. pyriformis var. tenuis (Penard, 1890, plate III, figs 47, 48) — g — D. pyriformis var. lacustris (Penard, 1899, plate 2, fig. 11) — h-m — variability oftypical form of D. pyriformis (Penard, 1902, p. 216) — n — D. pyriformis var. bryophila (Penard, 1902, p. 218) — o — D. pyriformis var. lacustris (Penard, 1902, p. 218) — p — D. capreolata (Penard, 1902, p. 223) — q — D. lanceolata (Penard, 1890, plate IV, fig. 59) — r-s — D. bacillifera (Penard, 1890, plate IV, figs 61−63) — t-v — D. lanceolata (Penard, 1902, p. 251).
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Fig. 8. Difflugia oblonga and related species from Cash and Hopkinson (1909, 1919). a-c — variation in typical form of D. oblonga (tableXVII, figs 1−3) — d-e — D. oblonga var. lacustris (table XIX, figs 1−2) — f-g — D. oblonga from Sphagnum habitats (table XIX, figs 3−4) — h-j — D. petricola (table XIX, figs 5−7) — k-m — D. lanceolata (table XIX, figs 9−11) — n — D. bacillifera (table XX, fig. 1) — o — D. oblonga var. bryophila (table LXI, fig. 9).
petricola-complex, D. bryophila-complex, and
D. linearis-complex, as well as two other species complexes which seem to be well defined in terms of both size and morphology, namely D. lanceolata-
complex and D. gigantea-complex.
Each species complex is here discussed in detail based on data from the E. Penard and C.G. Ogden collections in the NHM, London. We do not aim
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Fig. 9. Hypothetical phylogenetic scheme of Difflugia oblonga ultraspecies (after Stepanek, 1952 — modified): abbreviations show different forms distinguished by Stepanek (1952) in a single pond.
to make comprehensive revision of all published taxa related to each species complex. However, in many cases we discuss taxa not represented in the NHM collections but based instead on data from the literature.
Taxonomic revision of selected Difflugia species
All the species discussed below have a pyriform or elongate shell that is usually more than 100 pm in length (with the exception of few specimens of
D. linearis and D. gassowskii). Illustrations comprise light micrographs (LM), scanning electron micrographs and line diagrams. All light micrographs are originals of specimens from the Penard microscope
slide collection held at the NHM, London. All scanning electron micrographs are from the Ogden SEM collection held at the NHM, some of which are unpublished. Line diagrams are from different sources cited in the corresponding figure legends.
Difflugia oblonga Ehrenberg, 1838 species complex
The members of this group include D. oblonga,
D. lacustris, D. parva, and D. bacillifera and all of which have a similar size distribution and general appearance (Fig. 11, group 2- Fig. 12, e-g, i).
Difflugia oblonga Ehrenberg, 1838
Typical individuals are shown in Fig. 13. The
144 • Yuri Mazei and Alan Warren
Fig. 10. Selected Difflugia oblonga and its varieties from Chardez (1967, planche II). a — typical form of D. oblonga- b — D. oblonga var. gigantea- c — D. oblonga var. lacustris- d — D. oblonga var. cylindrus- e — D. oblonga var. elongata- f — D. oblonga var. parva- g — D. oblonga var. incondita- h — D. oblonga f. cyphodera- i — D. oblonga var. longicollis- j — D. oblonga var. angusticollis- k — D. oblonga var. stepaneki- l — D. oblonga var. rocki.
shell of Difflugia oblonga is elongate-pyriform with a long neck that is usually up to 1/3 of the shell length, sometimes clearly defined (Fig. 13b), sometimes not (Fig. 13a). The surface is rough to moderately smooth and covered with quartz particles of different sizes. The aperture is circular and surrounded by sand grains. Ogden measured 68 specimens of D. oblonga (Fig. 11), 67 of which were published (Ogden and Fairman, 1979- Ogden
and Hedley, 1980- Ogden and Zivkovic, 1983), one unpublished. The shell dimensions are as follows: length 128−263 qm, width 60−147 qm, aperture diameter 19−46 qm.
Difflugia parva (Thomas, 1954) Ogden, 1983
Variability ofD. parva according to C.G. Ogden is shown in Fig. 14. Ogden (1983) described this species as having a shell that is pyriform, tapering
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Fig. 11. Length-width measurements scatter plot on logarithmic scale of Difflugia with pyriform and elongate shells, based on C.G. Ogden’s measurements. 1−5 — size groups.
Note: D. linearis group includes three specimens of D. paulii- both species are shown in detail in Fig. 32.
evenly from the swollen and rounded aboral third to the aperture. Ogden measured 15 specimens of
D. parva (Fig. 11), 5 are published (Ogden, 1983- Ogden and Zivkovic, 1983) and 9 unpublished. Based on these data, the shell dimensions are: length 131 to 224 pm, width 61−103 pm, aperture diameter 19−40 pm.
Ogden (1983) separated D. parva from D. oblonga by its clean outline, relatively smooth surface and detailed cement pattern. The first two characters seem to be inappropriate given the high variability of the shell covering which depends on the material available in the environment (Stepanek, 1952). The importance of the cement pattern is also questionable (see: Mazei and Warren, 2012). Thomas (1954) described a new variety, D. oblonga var. parva (Fig. 10f), which is separated from the typical form only by its size. However, he assumed
that typical D. oblonga is 300−400 pm long compared to a size range of 169−256 pm for the new variety. Furthermore, neither Penard (1902) nor Cash and Hopkinson (1909) gave the length of D. oblonga (or
D. pyriformis) as being greater than 300 pm. Based on these data we conclude that D. parva (Thomas, 1954) Ogden, 1983 is ajunior synonym ofD. oblonga Ehrenberg, 1831.
Difflugia lacustris (Penard, 1899) Ogden, 1983
According to Ogden (1983) the shell of D. lacustris is transparent or hyaline, elongate, and cylindrical or slightly pyriform (Fig. 15). It is composed of small to medium-size pieces of quartz, diatom frustules and small siliceous flagellate cysts that together form a thin structure that is intermediate between smooth and rough. The aperture is usually circular and surrounded by
146 • Yuri Mazei and Alan Warren
Fig. 12. Comparative morphology of «typical» pyriform and elongate Difflugia ssp. (length 100−450 pm) from C.G. Ogden’s SEM collection. a — D. gigantea (SEM EM-12−587) — b — D. capreolata (SEM CZ-03. 181) — c — D. cylindrus (SEM CZ-04. 811) — d — D. pyriformis (SEM CZ-01. 155) — e — D. lacustris (SEM CZ-04. 630) — f — D. oblonga (SEM CZ-03. 198) — g — D. parva (SEM CZ-04. 365) — h — D. paulii (SEM CZ-06. 678) — i — D. bacillifera (SEM EM-06−731) — j — D. lanceolata (SEM CZ-04. 665) — k — D. petricola (SEM EM-12−457) — l — D. bryophila (SEM CZ-04. 041) — m — D. gassowskii (SEM CZ-05. 036) — n — D. linearis (SEM CZ-06. 677). Numbers after taxon names are NHM index numbers of SEM negatives. Scale bars: a — 100 pm, b-n — 30 pm.
small particles so that the margin is smooth. Ogden measured 23 specimens of D. lacustris (Fig. 11) all of which are published (Ogden, 1983): shell length 140−231 pm, shell breadth 63−94 pm, aperture diameter 26−42 pm.
Penard (1902) described D. lacustris as having an elongate shell, sometimes almost cylindrical, or broadened at the posterior end and tapering to the
aperture forming a neck (Figs. 7g- 16). The shell is usually covered by small sand grains sometimes with large sand grains near the aperture. The length of the shell is 160−180 pm. As discussed above, the nature of the shell surface is usually dependent on environmental factors. Here we follow Stepanek (1952) and regard D. lacustris as a junior synonym of D. oblonga.
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Fig. 13. Different specimens of Difflugia oblonga from C.G. Ogden’s SEM collection: a-b — lateral view (a — SEM CZ-03. 198, b — SEM EM-06−717), c — apertural view (c — SEM Z-15/951). Scale bars: a-b — 100 pm, c — 30 pm.
Difflugia bacillifera Penard, 1890
Ogden described D. bacillifera as having an elongate shell, the outline ofwhich is often concealed by adhered diatom frustules (Figs 17- 18). However, the number of frustules varies considerably among different specimens (Fig. 17). The aperture is circular and surrounded by small quartz particles. Ogden measured 66 specimens of D. bacillifera (Fig.
11), 57 ofwhich are published (Ogden, 1980- Ogden and Hedley, 1980) and 9 unpublished. The shell dimensions are as follows: length 117−198 pm, width 54−91 pm, aperture diameter 17−36 pm.
Penard (1890) described the shell of this species as being 150−170 pm long, elongate-pyriform in shape, usually transparent and covered with large diatom frustules (Figs 7, r-s- 19). Following Stepanek (1952), we consider D. bacillifera to be synonymous with D. oblonga.
Difflugia oblonga var. incondita Gauthier-Lievre and Thomas, 1958
This variety is characterized by its robust, ovoid-pyriform shell that is densely covered by angular sand grains to form rough surface (Figs 10g- 20).
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Fig. 14. Different specimens of Difflugia parva from C.G. Ogden’s SEM collection. a-e — lateral view (a — SEM CZ-04. 356, b — SEM CZ-04. 365, c — SEM CZ-03. 329, d — SEM CZ-03. 192, e — SEM CZ-І0. 975) — f — apertural view (SEM CZ-04. 357). Scale bars: a-e — 30 pm, f — 10 pm.
The maximum width is in the mid-region of the shell, which tapers conspicuously towards the aperture and slightly towards the posterior end. Measurements given by Gauthier-Lievre and Thomas (1958) are: length 195−245 pm, width 80−83 pm, aperture diameter 35−40 pm.
Difflugia oblonga var. incondita has never been studied in detail using morphometrical and/or SEM investigations. The size range matches closely with Difflugia oblonga senu Ogden. Differences in shape are not sufficiently significant for this taxon to be
valid. Thus, we here synonymise D. oblonga var. incondita with D. oblonga.
Difflugia oblonga f. cyphodera Jung, 1942
This form represents a slight deviation from the basic type (Fig. 10h). In his study of the variability of Difflugia in a single pond, Stepanek (1952) found a series of transitions from specimens with a slight indication of a bending of the test to the specimen figured by Jung (1942). Stepanek (1952) noted that a possible cause of the bending could be «…minute
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Fig. 15. Different specimens of Difflugia lacustris from C.G. Ogden’s SEM collection. a-e — lateral view (a — SEM CZ-04. 637, b — SEM CZ-04. 630, c — SEM CZ-04. 798, d — SEM CZ-05. 718, e — SEM CZ-07. 381) — f — apertural view (SEM CZ-04. 626) — g-h — structure of organic cement (g — SEM CZ-04. 631, h — SEM CZ-04. 655). Scale bars: a-f — 30 pm, g — 0.3 pm, h — 3 pm.
water currents at the time of the development of the young specimens, which was then moderately bent» (Stepanek, 1952- p. 24). Regardless, we believe that such charactersitics cannot be treated as taxonomically valid. Thus, we consider D. oblonga f. cyphodera to be a junior synonym of D. oblonga.
Difflugia pyriformis Perty, 1849 species complex
The members ofthis group include D. pyriformis,
D. capreolata, and D. cylindrus all of which have a similar size distribution and general appearance (Fig. 11, group 1- Fig. 12, b-d).
Difflugia pyriformis Perty, 1849
Ogden (1980) described the shell of D. pyriformis as opaque, tapering evenly from the aperture to about the mid-body position and curving in the aboral region (Fig. 21). The shell wall is composed of an assortment of quartz particles, arranged in
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Fig. 16. Different specimens of Difflugia lacustris from E. Penard’s slides. a-b — lateral view (slide 04.5.9. 125). Scale bars: 100 pm.
such a way that the outline is usually regular and the surface is intermediate between rough and smooth. The anterior region is usually covered with small pieces of quartz but occasionally has large, irregular particles. The apetrure is circular and surrounded by a regular arrangement of small quartz particles. Ogden measured 57 individuals of D. pyriformis, 43 of which were published (Ogden, 1980) and 14 unpublished, with the shell length ranging from 137 to 253 pm, shell breadth 88−153 pm, and aperture diameter 33−56 pm (Fig. 11).
Difflugia cylindrus (Thomas, 1953) Ogden, 1983
Ogden (1983) described the shell of D. cylindrus as usually opaque, almost cylindrical but tapering evenly from the aboral region to the aperture (Fig. 22, a, c). However, in addition to this shape we found in the Ogden SEM collection some specimens with a lanceolate shape (e.g. the width in the middle of the long axis of the shell being greater than that of the rest of the shell — see Fig. 22, b, d). The shell is composed mainly of medium to large pieces of quartz with the occasional diatom frustule on the rough surface, but the latter are seldom incorporated into the thick wall-structure. The aperture is irregular in both outline and composition, being roughly circular and usually surrounded by small particles but often incorporating medium particles that produce a jagged margin (Fig. 22e). Ogden measured 24 specimens of D. cylindrus (Fig. 11), 22 of which were published (Ogden, 1983), two unpublished. The shell dimensions are as follows: length 166−264 pm, width 80−130 pm, aperture diameter 34−50 pm.
This species was initially described by Thomas (1953) as a new variety ofD. oblonga (Fig. 10d). It is distinguished from the typical form by its elongate-cylindrical shape and covering of large sand grains. The shell dimensions are: length 220−260 pm, width 70−90 pm, aperture diameter 40−44 pm.
Both Ogden (1983) and Thomas (1953) highlighted the rough surface of the shell caused by the large particles incorporated in the shell wall. This could be a reason for the apparent difference in shape between D. cylindrus and D. oblonga (compare Figs 12c and 12d). Taking into the account that both taxa have the same size range (Fig. 11) and lack any clearly described permanent differentiating characteristics, we consider D. cylindrus a junior synonym of D. pyriformis.
Difflugia capreolata Penard, 1902
Ogden and Zivkovic (1983) described D. capreolata as having an opaque, thick, pyriform shell with a restriction of the neck in the anterior third before it expands in the posterior two-thirds (Fig. 23). The shell wall is composed of small to medium-size pieces of angular quartz. The aperture is circular and surrounded by a regular distribution of medium-size particles. Ogden measured two individuals of
D. capreolata, both published (Ogden and Zivkovic 1983- Ogden, 1984) with the shell length 225−237 pm, shell width 128−164 pm, aperture diameter 58−65 pm (Fig. 11).
In the original species description of D. capreolata, Penard (1902) underlined three main characteristics that distinguish it from D. pyriformis. Two are cell structures, i.e. the peculiarities of the nucleus and the pseudopodia. The third is shell shape, namely the constriction in the anterior third which was also described by Ogden and Zivkovic (1983). Having such a good morphological marker we retain this as a valid species until more data on its morphological variability are available. Photomicrogrphs of specimens from Penard’s slides are shown in Fig. 24.
Notes on D. oblonga Ehrenberg, 1838 and D. pyriformis Perty, 1849
As discussed above, the validity of both D. oblonga and D. pyriformis is questionable due to the lack of good original descriptions and the high variability of elongate and pyriform taxa of Difflugia. Until 1973 both names were widely used without any redescription of either species. Some authors (Leidy, 1879- Penard, 1890, 1902) preferred to use name 'pyriformis', whereas others (Cash and Hopkinson,
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Fig. 17. Different specimens of Difflugia bacillifera from C.G. Ogden’s SEM collection. a-f — lateral view (a — SEM CZ-02. 608, b — SEM CZ-01. 324, c — SEM EM-08−990, d — SEM EM-06−731, e — SEM EM-06−726, f — SEM EM-10−493). Scale bars: 30 pm.
1909- Stepanek, 1952- Gauthier-Lievre and Thomas, 1958- Chardez, 1967) applied the name 'oblonga' to these morphologically similar species. Chardez and Decloitre (1973) were first who proposed the idea to fix both names and characterize their typical features. Based on SEM observations and
morphometric analysis Ogden and Fairman (1979), and Ogden (1980) supported the findings of Chardez and Decloitre (1973), pointing out that although the shells of D. pyriformis and D. oblonga are similar in length, they differ significantly in both breadth and diameter of aperture (Fig. 11). Based on these
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Fig. 18. Different specimens of Difflugia bacillifera from C.G. Ogden’s SEM collection. a-b — apertural view (a — SEM CZ-01. 327, b -EM-06−728) — c — structure of organic cement (SEM CZ-01. 322). Scale bars: a, b — 30 pm, c — 1 pm.
findings Ogden (1980) proposed an elegant solution to the taxonomic problem which we accepted here. He wrote: «Cash and Hopkinson (1909) suggested that according to the rules of zoological nomenclature D. oblonga was the correct name to use for specimens of D. pyriformis under the law of priority. The problem of accepting this synonymy has been caused by subsequent reports under either specific name has resulted in a heterogeneous description. Several authors … recognized numerous varieties within this complex. The problem now is that we have clearly identified two species [in Ogden and Fairman, 1979- Ogden, 1980] that fall within the parameters of the descriptions of D. oblonga and D. pyriformis. It is almost certain that the type specimens of these species were never preserved., so that a comparison with these is out of question. Furthermore the synonymy proposed by earlier workers emphasizes that original descriptions are
inadequate. In resolving this situation. it seems unnecessary to create a new name when an accurate description of one of these species exists. I refer to Penard’s (1902) description of D. pyriformis [Fig. 25 shows the Penard’s vision of D. pyriformis]. This description is in such good agreement with the present description of D. pyriformis [Ogden, 1980] that they are considered to be conspecific. With regards to the other. species [D. oblonga in Ogden and Fairman, 1979], it would appear that the simplest way to avoid confusion is to retain the name that has already been used to describe it, that is D. oblonga, but emphasise that these two species are distinct and not synonyms» (Ogden, 1980- p. 464−466). We already accepted such an approach in our previous publications which showed both morphological (Bobrov and Mazei, 2004) and ecological (Mazei and Tsyganov, 2006) differences between these two species (Mazei and Warren, 2012).
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Fig. 19. Different specimens of Difflugia bacillifera from E. Penard’s slides. a-l — lateral view (a-c — slide 04.5.9. 82, d-f- slide 20. 12.8. 172, g-h — slide 20. 12.8. 173, i-j — slide 20. 12.8. 174, k-l — slide 20. 12.8. 175). Scale bars: 100 pm.
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Fig. 20. Different specimens of Difflugia oblonga var. inconditaa after Gauthier-Lievre and Thomas (1958). a-c — lateral view.
Difflugia bryophila (Penard, 1902) Jung, 1942 species complex
The members of this group include D. bryophila and D. gassowskii which have a similar size distribution and general appearance (Fig. 11, group 4- Fig. 12, l-m).
Difflugia bryophila (Penard, 1902) Jung, 1942
According to Ogden (1983), the shell of D. bryophila is brown, pyriform, with the sides usually tapering evenly to the aperture (Fig. 26), although the occasional specimen may be slightly miss-aligned, have a large particle obscuring the eventapering (Fig. 26b) or be almost cylindrical (Fig. 26c). The shell wall is composed mainly of a mixture of small to medium-size pieces of quartz and the occasional diatom frustule or siliceous flagellate cysts. The aperture is circular and surrounded by small particles. Ogden measured 46 specimens of
D. bryophila, 45 of which were published (Ogden and Zivkovic, 1983- Ogden, 1983, 1984), one unpublished (Fig. 11). The shell dimensions are as follows: length 83−141 pm, width 45−67 pm, aperture diameter 15−23 pm.
Difflugia bryophila differs from D. oblonga and D. pyriformis by its size (Penard, 1902 gave the length as 100 pm) and more transparent shell. The general shape is similar to both D. oblonga and D. pyriformis and varies according to the building material available in the environment.
Difflugia gassowskii (Gassowsky, 1936) Ogden, 1983
Ogden (1983) described this species as having a pyriform shell with a distinctly short neck about one-third of the body length, and a rounded aboral region (Fig. 27). The surface is rough and composed
of small to medium angular pieces of quartz. The aperture is circular. Ogden measured 23 specimens of D. gassowskii (Fig. 11) 21 of which are published (Ogden and Hedley, 1980- Ogden, 1983), two unpublished. Their dimensions are: shell length 81−120 pm, shell breadth 45−56 pm, aperture diameter 15−22 pm.
Ogden and Hedley (1980) referred to this species as D. longicollis since they raised the original D. piryformis var. longicollis of Gassowsky (1936) to the rank of species. Later, Ogden (1983) changed his decision because the name D. longicollis was used initially by Ehrenberg (1854) to describe specimens which now are not considered to belong to the genus Difflugia. Nevertheless, according to the International Code of Zoological Nomenclature the name is preoccupied.
Gassowsky (1936) originally described this variety under the name Difflugia oblonga var. longicollis as differing from the typical form by its very prominent neck and shell dimensions (length 72−116 pm, width 48−78 pm, aperture diameter 21−34.5 pm), which correspond well with the description of Ogden (1983). However, we do not believe that differences between D. gassowskii and
D. bryophila are taxonomically significant because the appearance of the neck is determined by the material available for its construction. Even among Ogden’s scanning electron micrographs, shells with or without a prominent neck can be observed (compare figures 26a and 26b). Thus, we treat D. gassowskii as a junior synonym of D. bryophila, based on the priority of the first description of
D. pyriformis var. bryophila Penard, 1902 and D. pyriformis var. longicollis Gassowskii, 1936 as well as their redescriptions as D. bryophila Jung, 1942 and
D. gassowskii Ogden, 1983, respectively.
Difflugia linearis (Penard, 1890) Gautier-Lievre et Thomas, 1958 species complex
The members of this group include D. linearis,
D. paulii, and D. nebeloides, all of which have a similar size distribution and general appearance (Fig. 11, group 5- Fig. 12, h, n).
Difflugia linearis (Penard, 1890) Gautier-Lievre et Thomas, 1958
Ogden (1983) characterized this species as having a shell that is transparent, flask shaped or elongate-pyriform, with a long, thin neck with parallel sides and a slightly swollen, rounded aboral region (Fig. 28). The surface is sometimes slightly uneven because of projecting particles, but generally it has a regular outline. It is composed of a mixture of
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Fig. 21. Different specimens of Difflugia pyriformis from C.G. Ogden’s SEM collection. a-b — lateral view (a — SEM CZ-01. 155, b — SEM CZ-08. 142) — c — apertural view (SEM CZ-04. 893) — d — structure of organic cement (SEM CZ-05. 680). Scale bars: a-c — 30 pm, d — 1 pm.
flattened pieces of quartz, small whole, flat diatom frustules, fragments of flattish frustules, small siliceous shell plates and globular flagellate cysts. The aperture is circular and usually surrounded by smal particles. Ogden measured 7 specimens of
D. linearis (Fig. 11), all of which were published (Ogden, 1980 — as D. lacustris- Ogden, 1983). The shell dimensions are as follows: length 96−108 pm, width 32−38 pm, aperture diameter 12−13 pm.
In his original description, Penard (1890)
referred to this taxon as D. pyriformis var. linearis and, based on his figures, the shell length varied from 60 to 100 pm (Fig. 7d). Gautier-Lievre and Thomas (1958) raised this taxon to species level and gave the shell dimensions as 90−105 pm long and 30−35 pm wide (Fig. 29, a, b). Although neither ofthese earlier descriptions emphasized the prominence of the neck, they are consistent with Ogden’s description in other regards, i.e. the transparent and elongated nature of the shell (Ogden, 1983).
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Fig. 22. Different specimens of Difflugia cylindrus from C.G. Ogden’s SEM collection. a-d — lateral view (a — SEM CZ-04. 411, b — SEM CZ-11. 360, c — SEM CZ-04. 811, d — SEM 8 711) — e — apertural view (SEM CZ-11. 356) — f-g — structure of organic cement (f — SEM CZ-04. 415, g — SEM CZ-8 710). Scale bars: a-e — 30 pm, f-g — 0.3 pm.
Difflugia paulii Ogden, 1983
According to Ogden (1983), D. paulii is characterised by its transparent, slender, elongate shell that tapers evenly from just anterior of the midbody region towards the aperture (Fig. 30). It is composed offlattish pieces of quartz to give a smooth
appearance. The aperture is circular and surrounded by small pieces of quartz. Ogden measured 4 specimens of D. paulii (Fig. 11) all of which were published (Ogden, 1983). The shell dimensions are as follows: length 119−130 pm, width 48−54 pm, aperture diameter 19−23 pm.
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Fig. 23. Different specimens of Difflugia capreolata from C.G. Ogden’s SEM collection. a — lateral view (SEM CZ-03. 181) — b — apertural view (SEM CZ-03. 190) — c — structure of organic cement (SEM CZ-03. 182). Scale bars: a-b — 30 pm, c — 3 pm.
This species was described previously as D. oblonga var. elongata by van Oye (1953) and Gau-thier-Lievre and Thomas (1958) (Fig. 29, c, d). The dimensions given by van Oye (length 140 pm, width 43 pm, aperture diameter 30 pm) and Gauthier-Lievre and Thomas (length 130−142 pm, width 38−40 pm, aperture diameter 28−37 pm) are in good agreement and correspond well with Ogden’s data. Ogden (1983) also noted that within a group of more elongated pyriform species, D. paulii appears to occupy a position mid-way between D. linearis and D. lacustris in terms of its shell length.
Davidova (2012) investigated the morphometry of D. paulii based on 20 specimens (all previous findings were more limited in terms of the number of specimens examined, e.g. van Oye (1953) examined one specimen, Ogden (1983) measured four, and Gauthier-Lievre and Thomas (1958) did not provided such information). The shell morphology and dimensions of the specimens examined by Davidova (2012) were consistent with Ogden’s (1983) description: shell length 110−125 pm, shell
length 44−51 pm, aperture diameter 18−24 pm (Fig. 31). Davidova (2012) also made morphometric comparisons with D. linearis and D. lacustris and concluded that the three are separate species.
Following a review of the available data, we do not consider the differences between D. paulii and D. linearis to be sufficiently significant for their separation at species level (compare figures 12h and 12n). Even in the figures of Gauthier-Lievre and Thomas (1958) the differences are not clear (compare figures 29, a-b and 29, c-d). We believe that the data of Davidova (2012) are also insufficient since she compared her 20 specimens of D. paulii with only three individuals of D. linearis. We applied the measurements of R. Davidova captured from her fig. 5 (Davidova, 2012- p. 43) and analyzed them with C.G. Ogden’s measurements. The resulting scatterplot is shown in Fig. 32 which reveals a continuum between the two species. Thus we conclude that there is insufficient evidence to support for the validity of D. paulii which we consider a junior synonym of D. linearis.
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Fig. 24. Different specimens of Difflugia capreolata from E. Penard’s slides. a-c — lateral view (a — slide 04.5.9. 88, b — slide 20. 12.8. 186, c — slide 04.5.9. 90) — d — dividing cells (slide 20. 12.8. 188). Scale bars: 100 pm.
Difflugia nebelotdes Gauthier-Lievre and Thomas, 1958
This species has not been redescribed since it was originally reported by Gauthier-Lievre and Thomas (1958) who described its shell as being transparent elongate-pyriform, circular aperture, shell length 118−140 pm, shell width 35−45 pm, aperture diameter 17−20 pm (Fig. 29, e, f). Based in its general appearance, this species closely resembles
D. linearis and D. paulii (Fig. 29), its shell dimensions being precisely between these two. Thus we consider
D. nebelotdes a junior synonym of D. linearis.
Difflugia gigantea Chardez, 1967) Ogden et Fairman, 1979 species complex
This species complex includes extra-large specimens with a pyriform or elongate shell and comprises three taxa: D. gigantea (Fig. 12a), D.
oblonga var. angusticollis and D. oblonga var. stepaneki.
Difflugia gigantea Chardez, 1967) Ogden et Fairman, 1979
Ogden and Fairman (1979) described this species as typically having a pyriform shell and a spherical fundus that tapers towards the aperture for about half the shell length (Fig. 33, c, d). The shell surface is smooth and constructed of medium-size pieces of flattened quartz. The aperture is circular or oval and surrounded by small particles of quartz. Other specimens from Ogden’s collection allow us to broaden the range of characters for this species to include those with a lanceolate shape and those that incorporate large sand-grains into the shell wall (Fig. 33, a, b). Ogden measured 10 specimens of D. gigantea, seven of which were published (Ogden and Fairman, 1979), three unpublished. The shell dimensions are as follows: length 341−480 pm,
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Fig. 25. Different specimens of Difflugia pyriformis from E. Penard’s slides. a-h — lateral view (a — slide 04.5.9. 138, b — slide 04.5.9. 124, c-g — slide 4.5.9. 132, h-j — slide 20. 12.8. 242, k-l — slide 20. 12.8. 268). Scale bars: 100 pm.
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Fig. 26. Different specimens of Difflugia bryophila from C.G. Ogden’s SEM collection. a-c — lateral view (a — SEM CZ-04. 041, b — SEM 30 054, c — SEM 3 824) — c — apertural view (SEM CZ-04. 047) — e — structure of organic cement (SEM CZ-04. 045). Scale bars: a-d — 30 pm, e — 1 pm.
width 168−231 pm, aperture diameter 55−84 pm.
Difflugia oblonga var. angusticollis Stepanek, 1952
Stepanek (1952) characterized this variety by its long, thin neck, and spherical test (Fig. 10j). The shell dimensions are as follows: length 315-
367.5 pm, width 175−210 pm, aperture diameter 42−70 pm. In the collection of C.G. Ogden’s SEM micrographs we found images of specimens that have a similar shape to D. oblonga var. angusticollis (Fig. 34). However, these specimens also had some notable peculiarities such as a conspicuous constriction between the neck and the fundus and an organic lip surrounding the aperture, which exclude them from being members of the genus Difflugia. Most likely they belong to Lagenodifflugia,
Pontigulasia or Zivkovicia. Consequently, we now have no conclusive evidence concerning the validity of D. oblonga var. angusticollis which must await further investigation by SEM and morphometric methods.
Difflugia oblonga var. stepaneki (Stepanek, 1952) Decloitre
Stepanek (1952) described this variety under the name D. oblonga var. vas (Fig. 10k) on account of its vase shape. It has an elongate test, slightly narrowed at the neck and widened toward the aperture. The covering on the shell surface is composed predominantly of medium-sized sand grains. Shell length 420 pm, shell width 160 pm, aperture diameter 88 pm. Chardez (1967) and Char-
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Fig. 27. Different specimens of Difflugia gassowskii from C.G. Ogden’s SEM collection. a-b — lateral view (a — SEM CZ-04. 623, b — SEM CZ-05. 036) — c — apertural view (SEM CZ-04. 619). Scale bars: a-b — 30 pm, c — 10 pm.
dez and Decloitre (1973) used another name for this taxon, D. oblonga var. stepaneki, without giving an explanation or citing Decloitre’s work. Thus, its validity is highly questionable.
Difflugia petricola Cash, 1909 species complex
This species complex includes broad-pyriform species belonging to group 3 of Fig. 11. It contains one species, D. petricola (Fig. 12k).
Difflugia petricola Cash, 1909
According to the description of Ogden and Hedley (1979), the shell of D. petricola is pyriform with a short neck that is about one-sixth of the shell length (Fig. 35). The aperture is circular and usually surrounded by a regular assortment of small quartz particles. The remainder of the shell is composed of randomly arranged sand grains and a few diatom frustules. The surface has a rough appearance. Ogden measured 89 specimens of D. petricola, all of which were published (Ogden and Fairman, 1979- Ogden, 1983, 1984). The shell dimensions are as follows: length 96−151 pm, width 58−99 pm, aperture diameter 20−36 pm.
Difflugia petricola is clearly distinguished from other species discussed in this paper by its broad-
pyriform shell. However, it has some transitions with other broad-ovoid species which will be discussed in the next article of this series.
Difflugia lanceolata Penard, 1890 species complex
This species complex is characterized by its lanceolate shape and contains one rather polymorphic species, D. lanceolata (Fig. 12j).
Difflugia lanceolata Penard, 1890
According to Ogden (1983) the shell of D. lanceolata is yellow or hyaline, lanceolate, being widest about two-thirds of the body-length from the aperture, rounded aborally and tapering evenly towards the aperture (Figs 36- 37). It is composed of small to medium-size, flattish pieces of quartz and some flat diatom frustules that are arranged in such a way as to make the shell wall appear characteristically thin and smooth. An angular piece of quartz may occasionally protrude from the surface but these are uncommon and limited to one or two in any shell. The aperture is circular and well defined because the rim has a thin covering of organic cement. Ogden measured 50 specimens of D. lanceolata, 42 of which were published (Ogden and Hedley, 1980- Ogden, 1983), eight unpublished:
162 • Yuri Mazei and Alan Warren
Fig. 28. Different specimens of Difflugia linearis from C.G. Ogden’s SEM collection. a-d — lateral view (a — SEM CZ-01. 161, b — SEM CZ-06. 677, c — SEM CZ-07. 828, d — SEM CZ-09. 115) — e — apertural view (SEM CZ-01. 241) — f — structure of organic cement (SEM CZ-06. 664). Scale bars: a-d — 30 pm, e — 10 pm, f — 3 pm.
shell length 85−163 pm, shell breadth 29−92 pm, aperture diameter 14−32 pm. There are some variations in shape and size found in C.G. Ogden’s SEM collection (Fig. 38, plate 59 in Ogden and Hedley, 1980).
Acknowledgements
This work was financially supported by the Russian Scientific Foundation (14−14−891)
and the award (to YM) from the Royal Society International Travel Grant Scheme (2009R1).
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Address for correspondence: Yuri Mazei. Department of Zoology and Ecology, Penza State University, Krasnaya str. 40, 440 026 Penza, Russia- e-mail: yurimazei@mail. ru

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