Ontogeny of the Upper Cambrian (Furongian) Olenid trilobite Protopeltura aciculate (Angelin, 1854) from Skåne and Västergötland, Sweden

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Abstract

Abstract:  The ontogeny of the trilobite Protopeltura aciculata (Angelin, 1854) is described on the basis of material from the upper Cambrian (Furongian) of Andrarum (Skåne) and Hjelmsäter (Västergötland), Sweden. P. aciculata is present in the Parabolina brevispina and Parabolina spinulosa zones. Protopeltura aciculata is represented by all stages of growth, from early protaspides to holaspides, although most of the specimens are disarticulated and precise degrees are unknown. The cranidia have therefore been allocated to five morphological groups. Cuticular sculpture of the cranidia changes throughout ontogeny. Large tubercles are present in earlier stages, disappear gradually in middle meraspid stages and are replaced with a very faint granulation. The transitory pygidium, relatively large and shield-shaped with upwardly and backwardly directed marginal spines in early meraspides, later becomes very small, triangular-shaped and lacking spines as a late meraspid and holaspid. The development of hypostomes and librigenae is also described. Protopeltura aciculata shows major intraspecific variations throughout development, especially regarding the pygidium where variation is much less constrained than in many other olenids. This high developmental plasticity may be a survival strategy for a trilobite living in a stressed environment. Protopeltura inhabited a dysoxic environment, possibly unusually prone to localised spreading of anoxic or toxic water. Some morphs may have been less vulnerable than others to such stresses, surviving by chance and thus enabling the species to continue.

The Furongian of Scandinavia is represented almost entirely by the Alum Shale Formation, a condensed succession of dark shales with calcareous concretions or limestone banks long known to yield an abundance of trilobites. The Alum Shales of Scandinavia have been extensively quarried in the past, providing many inland exposures, from which rich faunas have been collected. The Alum Shales are at their maximum thickness in Skåne, c. 80 m, of which the ‘traditional’ upper Cambrian comprises c. 50 m. The sequences are thickest and best exposed in the old quarries at Andrarum in the eastern part of Skåne (Westergård 1922) (Fig. 1), exploited between 1636 and 1912 (Andersson 1974). These quarries were described in detail by Tullberg (1880), Moberg (1910) and Westergård (1922). Many of the exposures are still available today. Good exposures are also found in other parts of Scandinavia, yielding abundant and well-preserved trilobites of the family Olenidae, which, along with Agnostida, constitute the bulk of the fauna of the upper Cambrian Alum Shales. In Skåne, the Alum Shale consists of black, finely laminated shales with bands or lenses of bituminous limestone. Trilobites from the Alum Shales of Sweden were described in detail by Anton H. Westergård in a series of papers written between 1922 and 1953 (Westergård 1922, 1942, 1944, 1947, 1948, 1950, 1953). Trilobites of the family Olenidae dominate the Furongian sequence. Olenid trilobites are of great use in stratigraphy. The rate of species turnover was very high with great geographical range, and seven zones based on olenids have been defined in the Furongian (Ahlberg 2003). Terfelt et al. (2008, 2011) reviewed the Scandinavian subdivision and elevated subzones to zonal status. Hence, the Furongian of Scandinavia is currently subdivided into 28 polymerid zones. In the Alum Shales, only one olenid genus and species is usually present at each level, though there are at least three species in parts of the Leptoplastus- and Peltura-bearing intervals (Ahlberg et al. 2006).

Figure 1.

 Sketch map of southern Scandinavia. The arrows indicate localities referred to in the text (Hjelmsäter in Västergötland and Andrarum in Skåne).

The olenids are extraordinarily abundant as individuals, but commonly found as monospecific assemblages. The environment they inhabited has been interpreted as being relatively deficient in oxygen (e.g. Andersson et al. 1985; Dworatzek 1987; Schovsbo 2000, 2001), and the olenids seem to have been well adapted to such stressful habitats. Fortey and Owens (1990) considered the olenids as specialised for nektobenthic life under conditions of low oxygen. Even though the olenids survived and thrived in a low-oxygen environment, they were, however, not restricted to dysoxic facies, especially during their later history. A study by Balseiro et al. (2011) from the Lower Ordovician of the Argentine Cordillera Oriental shows that olenids dominated both oxygenated and dysoxic environments. Similar patterns are found in other parts of the world (Nikolaisen and Henningsmoen 1985; Fortey and Owens 1991, 1992; Zylinska 2002).

Protopeltura aciculata (Angelin, 1854) is the earliest known pelturine. It is found in the Parabolina brevispina and Parabolina spinulosa zones. Protopeltura aciculata was first described by Angelin (1854) as a species of OlenusDalman, 1827 from Andrarum, Skåne. Brögger (1882) erected Protopeltura as a new genus and considered Angelin’s material to belong to this genus. Protopeltura aciculata was described by Westergård (1922) and discussed by Persson (1904) and Henningsmoen (1957).

Previous ontogenetic studies of olenids

Olenid ontogeny has previously been studied by Beecher (1893, 1895), Whitworth (1970), Clarkson and Taylor (1995), Clarkson et al. (1997), Månsson (1998), Lee and Chatterton (2007) and Tortello and Clarkson (2008). Early investigations into olenid ontogeny demonstrated that the morphological development mainly occurs in the meraspid period (Raw 1925). Previous ontogenetic studies of the pelturines are relatively few. Holtedahl (1910) illustrated incomplete juvenile cephala of Protopeltura holtedahliHenningsmoen, 1957. Different subspecies of Peltura scarabaeoides (Wahlenberg, 1818) have been described by Poulsen (1923), Whittington (1958), Hu (1964) and Bird and Clarkson (2003) from Bornholm, Denmark, Norway and Sweden. Tortello and Clarkson (2003) described the ontogeny of Jujuyaspis keideliKobayashi, 1936 from north-western Argentina, and they gave a thorough discussion of the ontogeny of some other pelturines.

Material and preservation

The material described in this paper is from Andrarum in Skåne and Hjelmsäter in Västergötland, Sweden (Fig. 1). The Hjelmsäter material was collected and donated to the collections at Lund University by John Ahlgren, and the material from Andrarum was collected at Westergård’s (1922) profile nr 5 by the authors in 2008. Westergård (1947) noted occasional findings of P. aciculata from southern Öland, Östergötland, Västergötland, Närke, Jämtland, Ångermanland in Sweden. Zylinska (2002) reported P. aciculata from the Holy Cross Mountains, central Poland, and Rushton (in Taylor and Rushton 1971) assigned a juvenile specimen from a borehole in the Merevale area in Warwickshire, central England, to P. aciculata.

In the examined material from Andrarum and Hjelmsäter, no other trilobites than P. aciculata were found. However, Westergård (1922) reported the rare occurrence of P. brevispinaWestergård, 1922 at Andrarum. In the Hjelmsäter material, we found occasional occurrences of the orthide brachiopod Orusia. In the material at our disposal, by far the majority of specimens belonged to meraspid to early holaspid periods. Protaspides are found, but they are comparatively uncommon; likewise, large holaspides are few. Articulated specimens of P. aciculata are rare, and those encountered are late meraspides or holaspides. Protopeltura aciculata is quite abundant in some layers, where they are often found crowded together and generally disarticulated. The trilobite remains are oriented in all directions in the plane of the bedding surface. The quality of preservation varies but is generally good. There is a strong variation of the ornamentation of the exoskeleton within the different stages of growth. This can partly be explained by the mode of preservation and perhaps to varying degrees of flattening. However, we have found a high degree of intraspecific variation in P. aciculata. This is discussed later in the text.

Repositories.  Illustrated specimens are housed in the Department of Earth and Ecosystem Sciences, Division of Geology, University of Lund (LO).

Systematic palaeontology

Subclass LIBRISTOMATA Fortey, 1990
Order PTYCHOPARIIDA Swinnerton, 1915
Suborder OLENINA Fortey, 1990
Family OLENIDAE Burmeister, 1843
Subfamily PELTURINAE Hawle & Corda, 1847

Genus PROTOPELTURA (Brögger, 1882)

Type species.  Protopeltura praecursor (Westergård 1909) (= P. acanthura Brögger), described by Brögger 1882, p. 106, pl. 1, figs. 14, 14a–c; pl. 2, figs. 13, 13a, from Naersnes in the Oslo area, Norway, SD by ICZN, 1958, opinion 499.

Protopeltura aciculata (Angelin, 1854)
Figures 2–6

Figure 2.

Protopeltura aciculata (Angelin, 1854). A. Anaprotaspis, latex cast, LO 11310t, Andrarum, × 115. B. Anaprotaspis, LO 11311t, Andrarum, × 105. C. Late anaprotaspis, LO 11312t, Andrarum, × 110. D. Early metaprotaspis, LO 11313t, Andrarum, × 115. E. Group 1 meraspid cranidium, LO 11314t, epon cast, Andrarum, × 100. F. Group 1 meraspid cranidium, LO 11315t, latex cast, Hjelmsäter, × 75. G. Group 2 meraspid cranidium, LO 11316t, Andrarum, × 75. H. Group 2 meraspid cranidium, LO 11317t, Andrarum, × 70. I. Group 3 meraspid cranidium, LO 11318t, Andrarum, × 55. J. Group 3 meraspid cranidium, LO 11319t, epon cast, Hjelmsäter, × 50. K. Group 3 meraspid cranidium, LO 11320t, Andrarum, × 55. L. Group 3 meraspid cranidium, LO 11321t, Andrarum, × 50. M. Group 3 meraspid cranidium, LO 11322t, internal mould with hypostome in place, Andrarum, × 60. N. Group 4 meraspid cranidium, LO 11323t, epon cast, Hjelmsäter, × 45. O. Group 4 meraspid cranidium with 1st thoracic segment, LO 11324t, latex cast, Hjelmsäter, × 30.

Figure 3.

Protopeltura aciculata (Angelin, 1854). A. Group 5 meraspid cranidium, LO 11325t, epon cast, Hjelmsäter, × 20. B. Group 5 meraspid cranidium, LO 11326t, epon cast, Hjelmsäter, × 25. C. Group 5 meraspid cranidium, LO 11327t, epon cast, Hjelmsäter, × 20. D. Holaspid cranidium, LO 11328, Andrarum, × 20. E. Pygidium, LO 11329t, Andrarum, × 100. F. Pygidium, LO 11330t, Andrarum, × 75. G. Pygidium, LO 11331, Andrarum, × 75. H. Pygidium, LO 11332, Andrarum, × 40. I. Pygidium with some thoracic segments, LO 11333t, latex cast, Hjelmsäter, × 15. J. Pygidia, LO 11334t, epon cast, Hjelmsäter, × 15. K. Pygidium, LO 11335t, epon cast, Hjelmsäter, × 15. L. Hypostome, LO 11336t, Andrarum, × 80. M. Hypostome, LO 11337t, Andrarum, × 60. N. Hypostome, LO 11338t, Andrarum, × 55.

Figure 4.

Protopeltura aciculata (Angelin, 1854). A. Librigena, LO 11339t, Andrarum, × 45. B. Librigena, LO 11340t, Andrarum, × 65. C. Cranidium with occipital spine, group 4, LO 11341t, Andrarum, × 35. D. Meraspis degree 6, group 3, LO 11342t, latex cast, Hjelmsäter, × 70. E. Meraspis, group 4, LO 11343t, Andrarum, × 35. F. Meraspis degree 11, group 5, LO 11344t, epon cast, Hjelmsäter, × 15. G. Holaspis, LO 11345t, latex cast, Hjelmsäter, × 8. H. Holaspis, LO 11346t, latex cast, Hjelmsäter, × 10. I. Holaspid thorax and pygidium, LO 11347t, epon cast, Hjelmsäter, × 15.

Figure 5.

 A–L, Protopeltura aciculata (Angelin, 1854). Morphological changes in dorsal exoskeleton during ontogeny, reconstructed from specimens in plates 1, 2 and 3. A. Anaprotaspis × 60. B. Early metaprotaspis, × 60. C. Group 1 meraspid cranidium, × 60. D. Group 2 meraspid cranidium, × 60. E. Group 3 meraspid cranidium, × 60. F. Group 3 meraspid cranidium, × 60. G. Group 3 meraspid cranidium, internal mould with hypostome, × 60. H. Group 3 meraspid cranidium, × 60. I. Group 3 articulated meraspid, × 60. J. Group 4 meraspid cranidium, × 60. K. Group 5 meraspid cranidium, × 50. L. Articulated holaspid, × 12.

Figure 6.

 A–G. Protopeltura aciculata (Angelin, 1854). Morphological changes in the pygidium during ontogeny, and an example of the intraspecific variation found in P. aciculata. A–G × 60. E–F, dorsal and lateral view of same individual.

  • 1854 Olenus aciculatus, Angelin, p. 44, pl. 25, fig. 6.

  • 1922 P. aciculata (Angelin); Westergård, pp. 169–170, 204, pl. 14, figs 3–12.

  • non 1922 P. aciculata (Angelin); Westergård, pl. 14, fig. 13.

  • 1922 P. aciculata pusilla n. var. Westergård, p. 171, pl. 14, figs. 14–17.

  • 1957 P. aciculata aciculata (Angelin 1854); Henningsmoen, pp. 222–223, pl. 3.

  • 1957 P. aciculata pusillaWestergård 1922; Henningsmoen, p. 223, pl. 3; pl. 23, figs 1–6.

  • non 2010 P. aciculata (Angelin); Rushton and Weidner, fig. 7c.

Type data.  As pointed out by Westergård (1922), the specimen described by Angelin (1854) from Andrarum is lost. Henningsmoen (1957) selected an axial shield figured by Westergård (1922, pl. 14, fig. 6), from Andrarum, Skåne, Sweden, as lectotype. The range of variation in P. aciculata is very broad (see below), and both Andrarum and Hjelmsäter accommodates both the subspecies P. aciculata aciculata (Angelin, 1854) and P. aciculata pusilla (Westergård, 1922). Accordingly, we propose that P. aciculata pusilla is a junior synonym of P. aciculata.

Diagnosis.  A Protopeltura species with cephalic axis quadrate to well rounded in front, preglabellar field virtually absent to present and moderately narrow, S1 and S2 distinct, S3 lightly impressed where visible, fixigenae approximately half as wide as glabella at ocular ridge, short palpebral lobe opposite S3, small eyes quite close to glabella, faint glabellar granulation. Postocular fixigenae 80–90 per cent of width of occipital ring. Genal spines of variable length, spine angle slightly obtuse to acute, 12 thoracic segments, pygidium small, subsemicircular without spines (emended from Henningsmoen 1957, p. 222).

Description of the adult.  The largest specimen is 8.7 mm in total sagittal length of the exoskeleton (Figs 3J–K, 4G–I, 5L, 6G). Oval in outline. The entire external shield is micro-granulated. Cephalon and axis rather convex, pleural regions more flat. The cranidium is subsemicircular in outline and moderately convex. Cranidium almost twice as broad (tr.) as long (sag.). Anterior border of cranidium is narrow (sag.) and straight. The glabella is rectangular with well-rounded anterior lateral and posterior lateral corners, about 1.3 times as long as wide, with nearly straight axial furrows. The glabella occupies 40 per cent of the total lateral width of the cranidium.

Three pairs of glabellar furrows are faintly impressed on the exoskeleton, more deeply so on internal moulds. S1 and S2 are long, sometimes slightly sinuous and curving strongly backwards medially. S3 is faintly discernable as small elongated pits. The occipital ring is 20 per cent of the total glabellar length, thickest medially, then thinning laterally. A prominent tubercle is directed backwards. Occipital furrow is straight and deep. Ocular ridges narrow and pronounced, rather straight, located between the preglabellar furrow and the S3 furrow. Palpebral lobes are short and located opposite S3. No eyes have been found, but the ocular incisures on the librigenae indicate that the eyes would have been small. The fixigenae are broadest posteriorly, with a straight posterior border. Postocular facial suture is divergent and convex. Posterior border furrow of the fixigenae is deep. Fixigena (singular) is 0.8 of the maximum glabellar width (tr.). The librigena is convex, broad with curving anterior and posterior margins. Genal spine is short and thin, directed outwards and curving backwards, reaching to about the posterior part of the first thoracic segment. The thorax is widest (tr.) at the 3rd to 5th segments. Thorax consists of 12 segments. The first axial ring is the widest, axis then narrowing evenly towards the pygidium. Axis is slightly less than one-third of total tr. width. Each axial segment displays the base of a broken off spine. Where the spine is preserved, it is longer than the length (sag.) of an axial ring. The articulating half-rings are well developed, of equal length (sag.) of the axial rings. Pleural furrows are deep, prominent and directed outwards and backwards from the inner anterior corner of each pleura to the outermost tip, rather straight and running diagonally backwards, only slightly curved at the end. Short pleural spines, directed backwards and slightly outwards.

The pygidium is very small and rather flat, rounded triangular in outline, with three axial rings and three pleurae. The axis is broad (tr.) and about 40 per cent of the total pygidial width. It tapers backwards, and the posterior end is rounded and reaches the narrow border. A well-defined articulating half-ring is present, almost as long (sag.) as the first axial ring of the pygidium. The pygidium lacks spines.

Remarks.  We found no adult hypostomes in our material. The one figured by Westergård (1922, pl. 14, fig. 13) does not, in our view, belong to this species. Angelin (1854) stated in his very short description that P. aciculata had 13 thoracic segments, but as Westergård (1922) pointed out, this was an error. At the locality and interval from where Angelin collected his specimen in Andrarum, no other species are found.

Ontogeny

Because of the fragmentary nature of the material, the development of cranidium, hypostome, librigena and pygidium is described separately. The glabella as measured is taken to include the occipital ring, but when measuring the total sagittal length, the occipital spine is excluded.

Protaspid development

The division of the protaspid period into an anaprotaspid and a metaprotaspid period, as proposed by Størmer (1942, p. 56, used for a detailed study of the protaspides of Olenus gibbosus pp. 81–88), is employed herein. The anaprotaspid period includes the earliest stages where the axis only has five segments, and the metaprotaspid period includes later stages where new axial segments are added, forming a protopygidium. Ross (1951) thought of the metaprotaspid period as beginning with a properly defined posterior cephalic border and thus a defined protopygidium, though not liberated as a true transitory pygidium. Olenid protaspides have earlier been described by, for example, Beecher (1893), Størmer (1942), Whittington (1958), Whitworth (1970), Clarkson and Taylor (1995), Clarkson et al. (1997), Månsson (1998) and Lee and Chatterton (2007). The general outline of these protaspides is semicircular with a pair of flanges on either side of the axis, providing the first indication of a protopygidium. The anterior spines, frontal knobs and dorsal tubercles – as described in Triarthrus latissimusMånsson, 1998– have not been found in any Cambrian olenid. The early stages in P. aciculata are similar to those of Olenus, Parabolina and Leptoplastus in general terms. There is a great resemblance to Leptoplastus angustatus (Angelin, 1854) (Description of ontogenies of L. angustatus and the other species of Leptoplastus recorded in Andrarum in Ahlberg et al. (2006) is in preparation for a forthcoming paper).

Anaprotaspid stage.  The anaprotaspides are cambered discs, almost completely circular in outline, somewhat truncated at the front and slightly tapering posteriorly (Figs 2A–C, 5A). Medium convex in profile. The sagittal length is 0.3 mm excluding spines, and the width (tr.) is also 0.3 mm. The protoglabella is spindle-shaped and expands slightly forwards, about one-third of the total transversal width, slightly <0.1 mm across, narrowing somewhat towards the rear. In early anaprotaspides, the protoglabella does not reach the posterior border, but in late anaprotaspides, it often does. The protoglabella shows faint segmentation, but five segments are defined by shallow furrows. The posteriormost segment projects slightly backwards. Some of the specimens show a distinct coarsely granulated pattern on the genal surfaces, and the protoglabella seems to be micro-granulated. This pattern of granulation is also shown in later stages of growth in P. aciculata. Two pairs of small marginal spines are present, projecting backwards. One pair is located at the posterolateral ‘corner’, and the other pair is located opposite SO. Neither ocular ridges nor palpebral lobes are visible.

Early metaprotaspid stage.  The specimens are of the same size as the anaprotaspid stage (0.3 mm in sagittal length and 0.3 mm in transversal width), circular in outline, but truncated anteriorly and posteriorly (Figs 2D, 5B). The protoglabella is about one-third of the transversal width, slightly more than 0.1 mm, somewhat broader than in the anaprotaspid stage and now of even width, reaching the anterior border. The protoglabella displays clear segmentation of five segments. There is a faint transverse border behind the fifth axial ring, marking off the protopygidium, but it is not yet separated (nor released). Protopygidial rings and furrows are indistinct. Two pairs of marginal spines are present. The base of a pair of intergenal spines is visible, and a pair of pygidial spines, pertaining to the protopygidium. Ocular ridges are now recognisable, placed close to the anterior margin, though they are not very well defined.

Late metaprotaspid stage.  We do not have any specimens with the pygidium fully formed, but not yet detached, or with more than one axial ring, (cf. Clarkson and Taylor 1995, figs 2e–h, 8d; Månsson 1998, figs 11d–e, 13d).

Remarks.  A comparison of protaspides from eight olenid species was given by Lee and Chatterton (2007). These authors suggest that the morphological differences in olenid protaspides are related to oxygenation condition. The protaspides from the Alum Shales are smaller in overall size, and most of them have a spindle-shaped axis, distinct anterior pits and a smaller protopygidium. The anterior pits are lacking in P. aciculata and in P. spinulosa (Wahlenberg, 1818) (Clarkson et al. 1997).

Development of cranidia of meraspid stages

As most of the material is disarticulated, precise degrees are often unknown. We have therefore allocated the cranidia of meraspid stages into five morphological groups, as done earlier by Whitworth (1970), Clarkson and Taylor (1995), Månsson (1998), Clarkson and Ahlberg (2002), and Tortello and Clarkson (2003). These groups are mainly based on the size and development of distinct morphological features. It is (sometimes) difficult to be certain whether cranidia of an intermediate size belong to meraspides or early holaspides. Such an assignment is inevitably subjective, especially because the species is in any case highly variable and whether the full complement of thoracic segments has actually been reached remains unknown, so some assumptions have to be made here.

Group 1.  The cephalon is 0.33–0.53 mm long and 0.33–0.53 mm wide, circular to semicircular in outline, well rounded anteriorly (Figs 2E–F, 5C). The glabella is parallel-sided, but can be either slightly narrowing or expanding forwardly, with five well-defined glabellar rings of even width. The glabella extends to the anterior margin. The occipital ring is triangular in shape; in larger specimens, it is strongly projecting backwards (Fig. 2F). It is uncertain whether it is the base of a broken off spine or whether the occipital spines that are found on later forms are not yet developed. The genal areas are coarsely granulated, while the glabella in some specimens is very faintly granulated and in others completely smooth. A pair of well-defined short straight ocular ridges is present at the anterior margin. The posterolateral corners of the cephalon are angular and provided with short spines, directed backwards. In some specimens, the spines are more slender.

Group 2.  The cranidia are semicircular in outline and highly convex, truncated anteriorly (Figs 2G–H, 5D). The length ranges from 0.35 to 0.55 mm and the width from 0.44 to 0.71 mm. The total sag. length of the cranidia belonging to this group is somewhat uncertain because more than half of the specimens do not have the occipital ring preserved. The glabella is of even width, with four rings, but the ring furrows are slightly shallower on the mid-glabella. Axial furrows are parallel. The glabella terminates before the anterior border, and a very narrow anterior border is present for the first time. Fixigenae are coarsely granulated, and the glabella is smooth or faintly granulated. Ocular ridges are prominent and transverse, then curving strongly backwards. A small intergenal spine is present. The posteriormost part of the occipital ring is in most of our specimens not completely preserved, but there appears to be the base a broken off spine.

Group 3.  The length varies between 0.52 and 0.70 mm and the width between 0.61 and 0.90 mm (Figs 2I–M, 5E–I). The cranidia are semicircular in outline, with a truncated straight anterior front. The glabella is subrectangular, widest at the posterior, tapering slightly forwards being rounded anteriorly. Four axial rings of even width, but S1 is shallower, and in some specimens, S1 is separated medially on the mid-glabella. Occipital ring with long slender spine that is generally broken off. The base of the occipital spine is quite stout. Posterolateral corners are almost right-angled with small spines that are now much reduced. The granulation on the fixigenae is even more prominent but not quite as coarse as in earlier stages. The ocular ridges are straight, then curving backwards, connected with a faint palpebral lobe. The ocular ridges show the same coarse granulation as the fixigenae. The S3 furrow is shallower than in earlier stages. One specimen is preserved as an internal mould with the hypostome attached (Figs 2M, 5G).

Group 4.  This group in particular shows major intraspecific variations. The outline is semielliptical, and the convexity is reduced (Figs 2N–O, 4C, E and 6J). The cranidia are between 0.64 and 0.92 mm long and 0.87 and 1.38 mm wide. The fixigenae are still densely granulated, but not as coarsely as in groups 2 and 3. The fixigenae expand in width (tr.) backwards. The posterior corners of the fixigenae are almost right-angled, and no genal spines are present. The glabella is subrectangular in outline, being rounded anteriorly and straight posteriorly. The glabellar furrows show great variation within this group. The S3 furrow is reduced into two straight shallow elongated pits. S2 furrow varies between being a furrow across the glabella and straight elongated pits with a shallow furrow between them; they can also be separated, and then S2 are curving slightly backwards. There are many intermediate specimens as well. S1 are convex straight in the mid-part and L1 being seen in some specimens. The occipital ring is convex posteriorly, and the occipital furrow is straight and deep. The occipital spine is absent in some specimen, and in some, it may be short and slender (Fig. 5J), while in others, it may be long and slender, at least as long as the total length of the cranidium (Fig. 4C). It seems to have been directed backwards and slightly upwards. The ocular ridges are situated further back than before, leaving a larger area between the ridges and the anterior border. The ocular ridges are only faintly granulated or are completely smooth. One complete but distorted specimen with seven thoracic segments (Fig. 4E) has been found; however, the thoracic segments are dislocated.

Group 5.  The cranidia are very adult-like, 1.15–1.39 mm long and 1.73–2.04 mm wide, semielliptical in outline (Figs 3A–C, 5K). The anterior border is straight. Glabella does not reach the anterior border furrow, and a thin preglabellar field is present for the first time. The ocular ridges have moved backwards, almost to the same position as S3. S3 are barely visible, indicated by faint impressions of elongated transverse pits. S2 are curving slightly backwards medially. S1 furrows are shallow, long and curved backwards medially. The glabella is barrel-shaped with well-rounded anterior lateral corners. The fixigenae are faintly micro-granulated. Palpebral lobes are prominent, located just in front of S3, ending just behind the S3 pits. Long slender occipital spine, broken off and cannot be measured, but appears to be shorter than in the previous group.

Development of the pygidium.  The protopygidium on the protaspides has already been noted (Figs 3E–K, 6A–G). It has not proved possible to match cranidia with pygidia of a known stage of development. The smallest complete specimen we found is a degree 6 (group 3). The intraspecific variation of the pygidia of P. aciculata is major regarding general morphology. Early meraspid transitory pygidia are fragile (and difficult to prepare without breaking them), and the spines are generally broken off. Including the articulating half-ring, the smallest liberated pygidium in our material is 0.24 mm long (sag.) and 0.40 mm wide (tr.) (Fig. 3E). It is semicircular in outline, with an articulating half-ring and 5 distinct axial rings. The pygidia, which probably belong to early to mid-meraspid stages, have four or five marginal spines. The spines are long and directed backwards and upwards. Some of the early pygidia show faint granulation of the axis. The largest pygidium is 0.5 mm in sagittal width and 1.6 mm in maximum transversal width, triangular in outline, with 3 axial rings. The smaller pygidia have long pleural spines directed upwards and backwards. The holaspid and late meraspid pygidia lack marginal spines (Figs 3H–K, 4F–I, 6G). The axis of juvenile pygidia shows prominent nodes or bases of broken off spines. As our material is mostly disarticulated, we cannot with certainty state when the marginal spines and axial nodes diminish and disappear. The axis increases in relative size from 25 per cent of the total sagittal width of the pygidium to 40 per cent and slightly more in holaspides. No terrace lines are visible on any of the pygidia.

Development of the hypostome.  Hypostome with simple central body and entire posterior margin (Figs 2M, 3L–N, 5G). A few stages in the development of the hypostome are shown in Figure 3L–N, taken from quite a large number of specimens. The largest and smallest specimens are of very similar appearance. The morphology does not seem to change much during ontogeny. In earlier stages, the central body is U-shaped and well rounded posteriorly. During growth, the posterior lobe narrows, giving it a V shape. In later stages, the posterior border is increasing in length (sag.). Many of the specimens are incomplete or partially buried, so measurements are difficult. The smallest hypostome has a highly convex median body, being most strongly pronounced posteriorly (Fig. 3L). The central body is prominent and undivided, forming an elongated ovoid with the anterior edge poorly defined. It is highly convex and tapers strongly posteriorly, being highest towards the rear. From the narrowest point (tr.) of the hypostome, there is a thin external rim that extends rearwards, following the posterior margin. The hypostome is narrowest at a point approximately a third of the distance from front to rear. Posterior border broad (sag.), about one-third of the total length of the hypostome in the larger specimens. The lateral and anterior border is narrower. The anterior part of the hypostomes is often not preserved, being buried or broken off. But in those better preserved, there is no evidence of anterior wings. The hypostome lacks maculae. The border furrow around the central body is laterally and posteriorly deep, but rather shallow anteriorly. There are no traces of sculpture on any of the hypostomes, and the surface appears to be completely smooth. In most respects, the hypostome of P. aciculata resembles that of Olenus and Parabolina.

Development of the librigenae.  There are very few librigenae preserved, and complete ones are extremely rare (Fig. 4A, B). Those found are all from Andrarum. The librigena starts out as a narrow rim (Fig. 4B) and then widens as the trilobite grows. The librigenae are coarsely granulated in earlier stages, and then the granulation gradually fades away. In late meraspid and holaspid stages, the librigenae are micro-granulated. A genal spine is present already in early meraspid stages. The spine does not change much during ontogeny, and it remains short and distinct, directed outwards and backwards. The genal spine reaches the second thoracic segment in adults. A shallow lateral border furrow outlines the librigenae.

Development of thoracic segments.  Isolated thoracic segments are not common in our material, and it is not usually possible to assign them to particular groups or to which position they have in the thoracic shield.

Remarks

Relationships

Fortey (1974) discussed the phylogenetic implication of early meraspid cranidia within Olenidae. According to Westergård (1922) and Henningsmoen (1957), the genus Protopeltura lasted into the Peltura minor Zone. Here, it lost its genal spines and developed into Peltura, which ranges into the Acerocare Zone. Protopeltura is not found however in the Leptoplastus Zone.

Summary of ontogenetic trends in Protopeltura aciculata

Glabellar furrows reduce from 3 to 1, and S1 becomes confined to the lateral regions only, S2 and S3 become faintly impressed elongated pits. The occipital ring is quite convex/inflated and triangular in the earlier stages, but becomes less so, and strap-shaped subsequently. The occipital spine, where present, becomes longer and slender. The coarse granulation on the fixigenae in early to mid-meraspides becomes finer until it disappears completely in the holaspides. The pygidium decreases in size relatively and becomes triangular in outline, and the spines likewise become shorter and broader at the base until they disappear. The relative dimensions of the cranidium change during growth, more so in the late meraspid to holaspid stages.

Intraspecific variation

In many groups of trilobites, morphology and size are closely coupled during ontogeny, and the forms and sizes of successive developmental stages are tightly constrained. Thus, it may be possible to recognise successive instars by measuring the dimensions (usually length and width) of individuals within a population and plotting these on a bivariate scattergram. Often, these graphs show distinct instar groupings or clusters, within which individuals are very similar in size and shape. Normally, it is the earlier growth stages that plot out most clearly in such clusters, and natural variation in the size of later stages obscures the distinction between them. Such patterns emerged clearly in an early work by Hunt (1967) on the agnostoid Trinodus elspethi (Raymond, 1924), in eodiscoids (Jell 1975, Zhang 1989, Zhang and Clarkson 1993; Cederstöm et al. 2009) and in many silicified trilobites, such as Scutellum (Chatterton 1971) and Dimeropyge (Chatterton and Speyer 1997), to name only a few. Such clustering of successive instar groupings on ontogenetic development seems to be common in trilobites generally, especially those of the Ordovician and later.

Within the Family Olenidae, certain genera and species follow the same pattern. Thus, clear instar groupings are apparent in Ctenopyge ceciliae (Clarkson and Ahlberg, 2002) and C. (Eoctenopyge) angustaWestergård, 1922 (Clarkson et al. 2003), and there is some tendency to grouping also in C. (Ctenopyge) gracilisHenningsmoen, 1957 (Clarkson et al. 2004). It is less distinct in P. scarabaeoides westergaardiHenningsmoen, 1957 (Bird and Clarkson 2003). Somewhat broad instar groupings are evident in J. keideliKobayashi, 1936 (Tortello and Clarkson 2003), but both in P. spinulosa (Wahlenberg, 1818) from Sweden and in Parabolina frequens argentina (Kayser, 1876) from Argentina, ontogenetic variation is considerable, some character states being much more advanced than others so that it is not possible to assign disarticulated sclerites to their correct meraspid degree. Variation among juveniles in P. frequens argentina was described as ‘formidable’ (Tortello and Clarkson 2008). And the same is very much true of P. aciculata and possibly even more so.

Perhaps the most arresting case of extreme variability in trilobites is that of the Furongian Dikelocephalus minnesotensisOwen, 1852 from the upper Mississippi valley, north central USA. This large and quite widespread asaphide can reach 40 cm in length, and so strong is the variability among adults that Ulrich and Resser (1930) erected no less than 25 species, which Hughes (1993, 1994) reduced to a single one. Here, there is no consistent pattern of clustering, but a continuous morphological variation between specimens both from the same bed and from different localities. There is no relationship between the variation in the trilobites and the enclosing lithologies. Only holaspides were available for study, because earlier stages were not preserved.

Hughes (1994, p. 58) discussed possible controls on variation in Dikelocephalus. He distinguished growth-related variation as one factor, in other words size/volume developmental constraints as the trilobite grew. A second factor was population-related variation, posing the question as to whether developmental plasticity in this case is a result of the palaeoenvironmental setting. But as there is no evidence of an unusually high environmental stress level in the northern Mississippi valley area during late Cambrian times, this does not seem very likely. From the genetic point of view, it seems that Dikelocephalus had a very flexible, in other words a poorly canalised, genotype – the alternative possibility of a series of genetically canalised polymorphs is not borne out by the evidence. A further factor is that in any case, Cambrian trilobites are generally much less developmentally constrained than those of the Ordovician. Olenellid genera, for instance, as has long been known, tend to intergrade, and many other Cambrian trilobites show a relatively high degree of morphological plasticity – this has been called the ptychopariid problem – where to draw the boundaries between species.

All these issues are important for interpreting the unconstrained variation in P. aciculata. There is, however, another possibility which we tentatively propose; that is, the high developmental plasticity that we see is actually a survival strategy for the species. The Alum Shales sea floor, by contrast with that in which Dikelocepahus lived, was undoubtedly a stressed environment for its inhabitants, being dysoxic and probably anoxic just below the surface. It may well have been toxic from time to time. If some potentially lethal event took place, a local spread of anoxic or poisoned water for example, then populations in which the individuals were all of very similar kind would be more likely to be wiped out completely than if they were highly variable. Some morphs in a more developmentally plastic population might survive by pure chance, and thus, the species would continue. There is a possible parallel here, albeit a distant one, with both the land snail Cepea nemoralisLinnaeus, 1758 and the Silurian mollusc Pterotheca (Clarkson et al. 1995). Cepea exhibits striking genetic polymorphism in its colour banding; it is actively preyed upon by thrushes which are highly selective about which morph they look for. They develop a ‘search image’ disregarding those morphs that fall outside this range, until the preferred morph become too scarce. Then, they have to begin to prey on another morph. In the long term, the balance between morphs remains stable, because a sequence of morphs is preyed on in turn, and the population of a previously sought morph will build up again when it is no longer the prime target. It was argued that the marine bellerophontiform Pterotheca was highly sought after by cephalopods (Clarkson et al. 1995), and marked polymorphic asymmetry confused their ‘search image’ in a very similar way. The difference between this kind of polymorphism and that of Protopeltura is that the stresses on the molluscs, with their voluminous flesh, are biological while those on the trilobites are more likely to be physicochemical.

If morphological plasticity, at all stages in development of Protopleltura, is indeed a response to stressed sea floor conditions, then why should the development of C. ceciliae, C. (Ctenopyge) gracilis and J. keideli be more ‘normal’, in other words why can discrete instar groupings be recognisable? Ctenopyge ceciliae is considered, on various grounds, to have been planktonic (Clarkson and Ahlberg 2002, Schoenemann et al. 2010). Jujuyaspis keideli was most likely pelagic, at least during the early meraspid stages; the later stages were probably nekto-benthic (Tortello and Clarkson 2003) as may have been C. (Ctenopyge) gracilis. Might it have been that the upper waters of the sea represented a less hazardous environment than the floor of the Alum Shale Sea, and thereby conduced to developmental ‘normality’? Such a concept is at least worthy of consideration.

Acknowledgments

Acknowledgements.  We thank Mats Eriksson and Brigitte Schoenemann for valuable discussions and Per Ahlberg and an anonymous referee for helpful suggestions on the improvement of the final manuscript. Alan Owen, Peter Doyle and Philip Lane have been of great assistance at the editorial level. We are grateful to Rita Wallén (Lund) and Nicola Cayzer (Edinburgh) for assistance with electron microscopy. Macro-photography of the trilobites was undertaken by Bill Crighton (National Museums of Scotland, Edinburgh). Financial assistance to ENKC was provided by the Synthesys Foundation and the Carnegie Trust for the Universities of Scotland.

Editor: Phil Lane

Ancillary