Pegmatothylakos manumii, McLoughlin, Bomfleur, Mörs & Reguero, 2016

McLoughlin, Stephen, Bomfleur, Benjamin, Mörs, Thomas & Reguero, Marcelo, 2016, Fossil clitellate annelid cocoons and their microbiological inclusions from the Eocene of Seymour Island, Antarctica, Palaeontologia Electronica 11 (1), pp. 1-27 : 13

Pegmatothylakos manumii sp. nov.

Figures 4.7-9; 8

zoobank.org/ 21970058-1A59-424A-855E-CE1BAEE14E9A

Holotype. NRMS089730 ( Figures 4.7-9; 8 ).

Type Locality, Stratum, and Age. Locality: IAA 1/ 90; ‘ Natica horizon’ within the Cucullaea I Allomember (Telm 5) of the La Meseta Formation; early Eocene.

Additional Material. NRMS 089734, locality: IAA 2/95; ‘ Natica horizon’ within the Cucullaea I Allomember (Telm 5) of the La Meseta Formation; early Eocene.

Etymology. After Professor Svein Bendik Manum (1926–2015), Norwegian palaeobotanist, who carried out the first major survey of fossil clitellate annelid cocoons.

Diagnosis. Cocoon ellipsoidal, <6 mm long. Pegmatine dark brown to black in reflected light, consisting of a semi-regular reticulum of girders enclosing circular, elliptical, or rounded-polygonal lumina mostly ~ 75–200 μm in diameter. Girders consisting of a core of fibrous or hackly material coated on the lateral and interior surfaces by multiple flattened strips of smooth, tightly overlapping threads. Hapsine amber-coloured, consisting of loosely interwoven slender threads.

Description. Cocoon ellipsoidal ( Figure 4.7 , 8.1 ); 4.6 mm in preserved length (estimated complete length ~ 5 mm), ~ 3 mm in equatorial diameter, circular in cross-section except where crushed; anterior end broadly rounded; posterior end damaged in all examples but potentially operculate ( Figure 4.8 ). Outer shell (pegmatine) consisting of a semi-regular reticulate network of girders enclosing roughly equidimensional (rounded-polygonal, broadly elliptical, or circular) lumina with maximum dimensions of 50–220 μm ( Figures 4.9 , 8.2 ). Girders consisting of two components—a core of brown fibrous or hackly material 20–35 μm thick ( Figure 8.6 ), and a lateral- and interior-surface coating of multiple flattened strips of subsequently secreted dark brown to black glossy dense threads that tightly overlap ( Figure 8.3-5 ) and locally bifurcate in complex arrangements ( Figure 8.7 ). Girders are ~ 50 μm thick and 50–80 μm wide. Rare spermatozoal fragments and other inclusions are entrapped between the laminar threads coating the inner surface of the pegmatine girders (described below).

Hapsine positioned to the interior side of the pegmatine but not obviously attached. Hapsine weakly developed, consisting of slender (2–8 μm diameter), amber-coloured, cylindrical, sparsely branched threads arranged in a loose, complex interwoven felt-like meshwork ( Figure 8.8 ).

Remarks. Only two specimens are available of this newly described taxon, but its unique architecture incorporating a robust pegmatine reticulum enables the species to be readily differentiated from all other fossil clitellate annelid cocoons. Attribution to Clitellata is based on the presence of a hapsine layer, apparently operculate character, and the sporadic occurrence of diagnostic spermatozoa inclusions embedded between the pegmatine filaments.

The pupal sacs of some Diptera, Coleoptera , Lepidoptera , and Neuroptera are enveloped by an external meshwork that is somewhat reminiscent of the pegmatine layer of Pegmatothylakos . However, such pupal casings are constructed in an essentially woven manner, i.e., having a succession of continuous threads that are superimposed in moreor-less opposite directions and subsequently connected. By contrast, the pegmatine in Pegmatothylakos has multiple layers of threads delineating individual rounded-polygonal lumina without any apparent hierarchical relationship in girder structure. We hypothesize that the formation of the pegmatine may—unlike that of a woven or otherwise coordinated construction—result, at least in part, from the self-organization of the girders on some ephemeral scaffold, possibly a mucous foam- or bubble-layer, at the time of cocoon secretion. Additional differences are the more variable and greater size of the lumina in the reticulum of insect pupal casings, and the much greater separation of the reticulum from the inner pupal sac (see, e.g., Eiseman and Charney, 2010; Holland, 2010).

Some insect eggs (especially those of lepidopterans) also have morphologies superficially similar to the reticulate structure of Pegmatothylakos ( Sourakov and Emmel, 1995; Dunn, 2010), and several examples of ornate Mesozoic insect eggs have recently been described in detail (e.g., Pott et al., 2008; Heřmanová and Kvaček, 2010; Heřmanová et al., 2013; Fisher and Watson, 2015). However, both modern and fossil insect eggs have complex wall anatomies and surface morphologies with reiterating patterns ( Hinton, 1970, 1981; Ren, 1992; Wolf and Reid, 2001; Fisher and Watson, 2015) that allow their differentiation from annelid cocoons.

Figures

FIGURE 4. Light micrographs of early Eocene clitellate annelid cocoons from Seymour Island. 1–3, Burejospermum seymourense sp. nov. (NRMS089727). 4–6, Burejospermum punctatum sp. nov. (NRMS089728). 7–9, Pegmatothylakos manumii sp. nov. (NRMS089730). 1, 4, 7, Lateral views of cocoons (posterior to left); g = equatorial girdle. 2, 5, 8, Views of posterior end of cocoons showing opening left by detachment of operculum. 3, 6, 9, Enlargements of cocoon wall exterior showing pale felt-like hapsine covering in B. seymourense (3), relatively smooth surface in B. punctatum (6) and reticulate pegmatine of P. manumii (9). Scale bars represent 1 mm in 1, 2, 4, 5, 7, 8; 100 µm in 3, 6, 9.

FIGURE 5. Scanning electron micrographs of Burejospermum seymourense sp. nov. (NRMS089727). 1, Cocoon in lateral view. 2, Details of typical hapsine threads. 3, Detail of dense hapsine threads over girdle region. 4, Elliptical secreted plate-like structures on exterior of hapsine. 5, Broken cocoon wall in cross-section showing solid alytine (lower) and thread-like hapsine (upper). 6, Detail of plate-like secretion on exterior of hapsine. Scale bars represent 1 mm in 1; 100 µm in 2; 50 µm in 3, 4; 25 µm in 5, 6.

FIGURE 6. Computed tomographic images of a Burejospermum seymourense cocoon wall (NRMS089729) generated from Synchrotron-radiation-based X-Ray tomographic microscopy (SRXTM) at the TOMCAT beamline of the Swiss Light Source at the Paul Scherrer Institute, Switzerland. 1, Isosurface rendering of cocoon’s external surface showing mineral grains embedded in hapsine. 2, Isosurface rendering of cocoon’s internal surface showing creasing caused by alytine threads. Arrow indicates the position of a hollow tube within the alytine. 3, 4, Longitudinal orthoslice sections, at different focal planes, of a tube within the alytine showing pseudosegmentation. 5–8, Translucent volume rendering of a tube within the alytine imaged at different focal planes and magnifications to highlight the transverse to chevron-shaped thread arrangement lining the tube wall. 9, Isosurface rendering of hapsine outer surface showing details of the complex arrangement of hirudoin threads. 10, Transverse orthoslice section of the cocoon wall showing the near-solid alytine layer (bottom) and mesh-like hapsine layer (top). 11, Isosurface rendering of interior alytine wall showing an embedded spermatozoal nuclear region. 12, Colour-inverted rendering of Figure 6.11. 13, Volume rendering of the cocoon wall showing numerous mineral (white–yellow) inclusions. 14, Oblique translucent volume rendering of the cocoon wall showing the distribution of mineral grains mainly in the outer hapsine layer. Scale bars represent 100 µm in 1, 2, 10, 13, 14; 50 µm in 9; 25 µm in 3–7; 10 µm in 8; 5 µm in 11, 12.

FIGURE 7. Scanning electron micrographs of Burejospermum punctatum sp. nov. (NRMS089728). 1, Cocoon in lateral view. 2, Details of sparse hapsine threads embedded in alytine surface. 3, Detail of typical cocoon surface showing pitting. 4, Detail of girdle region showing granular microtexture and a single surface pit. 5, Detail of outer alytine surface showing cleft and fold structures (arrowed). 6, Cross-section of cocoon wall showing laminated architecture. Scale bars represent 1 mm in 1; 100 µm in 3, 5; 10 µm in 2, 4, 6.

FIGURE 8. Scanning electron micrographs of Pegmatothylakos manumii sp. nov. (NRMS089730). 1, Cocoon in lateral view. 2, Enlargement of robust reticulate pegmatine covering thread-like hapsine. 3, Enlargement of areole in pegmatine reticulum showing underlying mesh-like hapsine. 4, Enlargement of girders forming pegmatine showing hackly inner zone and smoothly welded threads lining girder margins. 5, Detail of hackly and smooth threads in pegmatine girders. 6, Broken pegmatine girder showing irregular internal structure. 7, Enlargement of interior surface of pegmatine girder showing smooth threads with irregular branching and orientation. 8, Enlargement of hapsine threads. Scale bars represent 1 mm in 1; 250 μm in 2; 100 μm in 3, 4; 25 μm in 5–8.

FIGURE 9. Spermatozoa and bacteria preserved embedded in the innermost layer of the alytine wall of Burejospermum seymourense sp. nov., NRMS089729 (1–12); Burejospermum punctatum sp. nov., NRMS089728 (13); and Pegmatothylakos manumii sp. nov., NRMS089730 (14). 1, Overview of cocoon inner surface showing a range of elongate spermatozoa and elliptical–reniform bacteria. 2, Spermatozoon acrosome (white arrow) with swollen tip (probably containing the acrosome vesicle) and apical button (black arrow). 3, Enlargement of a spirally organized detached acrosome. 4, Thin sheet-like innermost layer of alytine draped over mineral inclusion (top) and entombing numerous elliptical bacteria. 5, Several spermatozoal nuclear regions, one with an attached whip-like flagellum (white arrow). A pair of dimpled elliptical bacteria are also present in the upper left (black arrow). 6, Enlargement of a portion of a spermatozoon flagellum showing slightly beaded structure. 7, Enlargement of the nuclear and mitochondrial region of a spermatozoon showing granular ornamentation and swellings in the anterior portion of the attached flagellum. Reniform bacterium also present in upper right (white arrow). 8, Several spermatozoal flagella showing indistinct spiral architecture. 9, Nuclear (white arrow), mitochondrial (black arrow) and anterior flagellar (hollow arrow) regions of a spermatozoon. 10, Enlargement of a flagellum showing beaded structure that probably reflects helical architecture. 11, Enlargement of Figure 9.9 showing details of nuclear (n), mitochondrial (m) and anterior flagellar (f) regions. 12, Overlapping elliptical bacterium (b) and flagellate spermatozoon. 13, Elongate coiled acrosome (a) and slender flagellum (f) of separate spermatozoa. 14, Nuclear (n) and flagellar (f) regions of a spermatozoon. Scale bars represent 10 µm in 1, 4, 5, 13, 14; 2 µm in 2, 3, 7–9; 1 µm in 6, 10–12.