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HERBIVOROUS AND DETRITIVOROUS ARTHROPOD TRACE FOSSILS
ASSOCIATED WITH SUBHUMID VEGETATION IN THE MIDDLE
PENNSYLVANIAN OF SOUTHERN BRITAIN
Author(s): HOWARD J. FALCON-LANG, CONRAD LABANDEIRA, and RUTH KIRK
Source: PALAIOS, 30(3):192-206.
Published By: Society for Sedimentary Geology
URL: http://www.bioone.org/doi/full/10.2110/palo.2014.082
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PALAIOS, 2015, v. 30, 192–206
Research Article
DOI: http://dx.doi.org/10.2110/palo.2014.082
HERBIVOROUS AND DETRITIVOROUS ARTHROPOD TRACE FOSSILS ASSOCIATED WITH SUBHUMID
VEGETATION IN THE MIDDLE PENNSYLVANIAN OF SOUTHERN BRITAIN
HOWARD J. FALCON-LANG,1,2 CONRAD LABANDEIRA,3,4 AND RUTH KIRK1
1Department of Earth Sciences, Royal Holloway, University of London, Egham, Surrey TW20 0EX, UK
2Forschungsstelle fu¨r Pala¨obotanik, Geologisch-Pala¨ontologischen Institut, Westfa¨lische Wilhelms-Universita¨t Mu¨nster, Hindenburgplatz 57, 48143 Mu¨nster, Germany
3Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, , Washington D.C. 20560, USA
4Department of Entomology and BEES Program, University of Maryland, College Park, Maryland 20742, USA
e-mail: h.falcon-lang@es.rhul.ac.uk
ABSTRACT: We describe plant–arthropod associations from the Middle Pennsylvanian (late Bolsovian–early Asturian)
Pennant Sandstone Formation of southern Britain. Our material comprises calcified cordaitaleans and tree-fern axes,
preserved in braided channel deposits, and interpreted as remains of subhumid riparian vegetation distinct from that of coeval
coal swamps. The first plant–arthropod association, attributed to herbivorous insects, comprises cambial damage to
cordaitalean leafy branches, resulting in traumatic wound response. The second and most widespread association, attributable
to detritivorous oribatid mites, includes tunnels and galleries containing widely scattered, clustered, or densely packed
microcoprolites within the inner root mantle of marattialean tree ferns and cordaitalean trunks and branches. Diameter data for
tunnels and microcoprolites are multimodal, recording four or five instars of oribatid mites that parallel instar-based fecal pellet
and body lengths in modern taxa. The third association attributed, possibly, to an arthropleurid, comprises a single, very large
(19 3 14 mm) coprolite. Included plant fragments support a previous conjecture that arborescent lycopsids formed part of this
iconic arthropod’s diet. Mucus-lined burrows within the macrocoprolite imply that fecal material was processed by annelids.
The high diversity and frequency of plant–arthropod associations are unusual for Mid-Pennsylvanian time, and may reflect
previously undetected interactions in those ecosystems that lay outside ‘‘coal forest swamps.’’
INTRODUCTION
Mites and insects (arthropods) are the two most diverse groups of
organisms that interact with land plants today. Around the time of their
Early Devonian origin (Jeram et al. 1990; Norton 1994; Brett et al. 1996;
Labandeira 2006), these organisms appear to have been predominantly
predatory, but at an early evolutionary stage, they widely adopted
detritivory (consumption of dead plant tissues) as an alternative mode of
feeding (Labandeira et al. 1997a, 1997b; Norton 1985; Engel and Grimaldi
2004) and occasional herbivory (Kevan et al. 1975; Labandeira 2007). The
transition from a predatory to a plant-based diet was undoubtedly aided
through association with cellulytic and lignin-feeding fungi (Taylor and
Osborn 1996; Renker et al. 2005), although evolution of the latter group
may have been delayed until the end of the Carboniferous (Floudas et al.
2012). Herbivory (consumption of living plant tissues) was very limited
during the Devonian (Labandeira 2007, 2013), and only significantly
expanded several tens of millions of years later, during the Late
Mississippian to Early Pennsylvanian, and primarily among insects
(Labandeira 2007; Iannuzzi and Labandeira 2008).
In late Paleozoic permineralized plant assemblages (e.g., fossil wood
and peat), oribatid and other mites, have left an extensive record of
detritivory (Stidd and Phillips 1982; Rex 1986; Chaloner et al. 1991; Goth
and Wilde 1992; Zavada and Mentis 1992; Labandeira et al. 1997a;
Ro¨ßler 2000; Tomescu et al. 2001; Hueber and Galtier 2002; Kellogg and
Taylor 2004; Feng et al. 2010; D’Rozario et al. 2011; Slater et al. 2012).
At this time, oribatid mites played a major role in recycling dead organic
matter (Oconnor 1982; Hansen 1999; Schneider et al. 2005; Maraun et al.
2009), occurring as diverse microvores in soil, plant litter, and other
habitats rich in decomposing plant substrates (Hirst 1923; Krivolutsky
and Druk 1986; Bernini 1986; Norton et al. 1988; Kethley et al. 1989).
The late Paleozoic dominance of oribatid mite detritivory is attributable
to their early origin and adaption to dead plant-tissue substrates (Norton
1994; Maraun et al. 2004; Jeyaprakash and Hoy 2009; Dunlop and Selden
2009), and their relatively high, incumbent diversity and abundance
(Bernini 1986; Schaefer et al. 2010), based on elevated modern diversities
(Schatz 2004; Maraun et al. 2007).
The oldest unequivocal evidence consistent with oribatid mite
detritivory is found in Lower and Middle Devonian deposits, in which
microcoprolites and traumatic plant tissue damage (Kevan et al. 1975;
Labandeira 2006) are locally buttressed by mite body fossils preserving
distinctive mouthparts (Hirst 1923; Norton et al. 1988) and surface
ornamentation (Norton et al. 1988; Kethley et al. 1989); however,
oribatid mite detritivory may have originated even earlier in the Silurian
(Hagstro¨m and Mehlqvist 2012). More generally, oribatid mite detritiv-
ory is recorded in the late Paleozoic fossil record by populations of
spheroidal, ovoidal, and short-ellipsoidal microcoprolites found in
remains of dead plant tissue (Labandeira et al. 1997a; Kellogg and
Taylor 2004; D’Rozario et al. 2011; Slater et al. 2012), their overall shape
and dimensions consistent with those of extant oribatid mite micro-
coprolites (Rusek 1975). The most detailed data for oribatid detritivory
exists in the Pennsylvanian peat deposits of tropical Euramerica (coal
balls), where the dead material of virtually every known plant group
contains such microcoprolites (e.g., Scott 1977; Cichan and Taylor 1982;
Scott and Taylor 1983; DiMichele and Phillips 1994).
By contrast, evidence for insect detritivory has a rather spotty fossil
record. Although the earliest insect body fossils are from the Early and
Published Online: March 2015
Copyright E 2015, SEPM (Society for Sedimentary Geology) 0883-1351/15/030-192/$03.00
Middle Devonian (Shear et al. 1984; Labandeira and Beall 1990),
compelling evidence for insect detritivory is rare. Such evidence, which is
mostly of Pennsylvanian and younger age, consists, almost exclusively, of
borings of considerably larger diameter than those of oribatid mites,
which penetrate cortical and medullary trunk tissues, yet lack the live-
tissue response that would indicate herbivory (Rothwell and Scott 1983;
Weaver et al. 1997; Labandeira and Phillips 2002, D’Rozario et al. 2011).
Judging from this fossil record of borings and related damage of dead
plant tissue, insects appear to have invaded different plant tissue types
compared to mites. The smaller mites preferred more hardened,
sclerenchymatous structural tissues, particularly wood and periderm,
whereas the larger insects targeted softer, more nutritious, parenchyma-
tous tissues such as branch piths, cambiums and other meristematic
tissues, seeds, and the interiors of leaves, through borings, seed predation,
galling, and leaf mining (Labandeira 2006, 2007, 2013).
Varied modes of herbivory first appeared among insects during the
Late Mississippian to Middle Pennsylvanian (Labandeira 2007, 2013).
This evidence includes external foliage feeding (Iannuzzi and Labandeira,
2008; Labandeira 2013), piercing and sucking (Labandeira and Phillips
1996a), galling (Amerom 1973; Labandeira and Phillips 1996b), seed
predation (Jennings 1974), and oviposition (Be´thoux et al. 2004).
However, the distinction between herbivory and detritivory is not always
clear in these mid-Carboniferous assemblages. For example, some
typically detritivorous insect borings in Late Pennsylvanian tree ferns
(Rothwell and Scott 1983, Labandeira and Phillips 2002) appear to have
continued into the upper, live portion of the trunk, where they induced a
limited hypertrophic and hyperplasic tissue response typical of herbivory
(Labandeira and Phillips 2002).
As emphasized above, almost all work on Pennsylvanian plant–
arthropod interactions has focused on perhumid tropical forest mires,
based on coal ball material (DiMichele and Phillips 1994) with little or no
explicit documentation of patterns in the subhumid riparian vegetation
that it is now inferred to have widely covered the Pennsylvanian tropics
(Falcon-Lang 2003; Feldman et al. 2005; DiMichele et al. 2010; Falcon-
Lang et al. 2009, 2011a; Bashforth et al. 2014), especially during cooler
and drier glacial phases (Falcon-Lang 2004; Falcon-Lang and DiMichele
2010). In this contribution, we document more fully the feeding biology of
early Middle Pennsylvanian-age insects, oribatid mites, and other
arthropods, and focus on evidence specifically from subhumid riparian
ecosystems, through an analysis of their borings and associated
coprolites.
GEOLOGICAL CONTEXT
Evidence for plant–arthropod associations reported here occurs within
collections of calcic-permineralized fossil plants from the Pennant
Sandstone Formation (Warwickshire Group) of southern Britain
(Falcon-Lang et al. 2012).
Fossil Localities
Specifically, material comes from twelve localities near Bristol and
Caerphilly (Fig. 1A–C). The Bristol localities are Conham Quarry
(51u26950.940N, 2u32917.480W); Hanham Quarry (51u25942.380N,
2u30928.060W); Oldbury Court quarries (51u29918.050N, 2u31955.280W);
Hambrook (51u30917.370N, 2u30951.140W); Rock Quarry (51u26923.110N,
2u32945.060W); Winterbourne Quarry (51u30949.270N, 2u30904.330W);
Conygar Quarry, near Clevedon (51u26945.740N, 2u50904.320W); and the
Severn Tunnel excavations (51u35922.750N, 2u43900.110W). The Caer-
philly localities are Caerphilly Common Quarry (51u36946.600N,
3u13903.470W); Treforest Quarry, near Pontypridd (51u34954.930N,
3u18943.580W); Bute Quarry, Pwllypant (51u36912.480N, 3u14904.860W);
and Six Bells Colliery, Abertillery (51u43950.570N, 03u07952.880W).
Stratigraphy and Facies
Across this study area, the Pennant Sandstone Formation is 700–
1350 m thick and dominated by very thickly bedded, coarse-grained,
pebbly sandstone units, which show channels many tens to hundreds of
meters wide, trough cross-bedded channel-fills that fine upward, and
large-scale tabular cross-bedding (Jones and Hartley 1993; Waters et al.,
2009; Falcon-Lang et al. 2012). These facies are indicative of the low-
sinuosity channels of very large, sandy braided rivers (Jones and Hartley
FIG. 1.—Geological context of sample localities, modified from Falcon-Lang et al. (2012). A) British Isles showing the location of the two main collecting areas near
Bristol and Caerphilly, in the context of late Westphalian paleogeography. Abbreviations and symbols: VDF, Variscan Deformation Front; gray, highlands; white,
alluvial lowlands. B) Bristol, southern England, showing collection sites as follows: 1 5 Conham Quarry; 2 5 Hanham Quarry; 3 5 Oldbury Court Quarry; 4 5
Winterbourne; 5 5 Conygar Quarry; and 6 5 Portskewett tunnel excavations. C) Caerphilly, South Wales, showing collection sites as follows: 7 5 Treforest Quarry; 8 5
Bute Quarry, Pwllypant; 9 5 Abertillery coal mine; and 10 5 Caerphilly Common Quarry.
PENNSYLVANIAN PLANT–ARTHROPOD ASSOCIATIONS IN SOUTHERN BRITAIN 193P A L A I O S
1993). Paleocurrent data has a strong north and northeasterly mode,
suggesting rivers drained the rising Variscan Orogenic belt to the south
(Gayer and Jones 1989). This is supported by sediment petrology and
structural studies that show that the edge of the Variscan Deformation
Front lay only a few tens of kilometers south of our study areas
(Leverridge and Hartley 2006; Fig 1A).
Geologic Correlation and Age
The Cambriense Marine Band (a regional stratigraphic marker bed),
which passes through the diachronous base of the Pennant Sandstone
Formation (Stubblefield and Trotter 1957), is of mid-Bolsovian age
(Waters et al. 2009), whereas the diachronous top of the formation is
late Bolsovian near Bristol (Pendleton et al. 2012) rising to mid-
Asturian near Caerphilly (Cleal 1997, 2007; Falcon-Lang et al. 2012).
Consequently, based on interregional correlations (Heckel 2008;
Davydov et al. 2010; Falcon-Lang et al. 2011b; Waters and Condon
2012), the fossils are of early Middle Pennsylvanian (mid-Moscovian)
age (Fig. 2).
Taphonomy of Fossil Plant Collections
Although fossil material reported here was mostly collected between
1868 and 1924, the sedimentologic and stratigraphic context of each
historic collection site within the Pennant Sandstone Formation is well
constrained. Based on field notebook entries made at the time of
collection and other archival data (see Crookall 1931; Falcon-Lang et al.
2012), all material originated as allochthonous channel-lag assemblages.
This is supported by field visits to several of the localities, where similar
material can still be collected from channel-lag deposits today, occurring
as water-worn, calcic-permineralized pebbles and cobbles.
MATERIAL AND METHODS
The material comprises 171 petrographic thin sections scattered
through various museum collections. Direct observations and museum
archival records suggest that these thin sections represent , 72 separate
fossil specimens (Falcon-Lang et al. 2012). Some specimens are
represented by a solitary section only, but for others, sets of multiple,
FIG. 2.—Stratigraphic chart showing the position and age of the Pennant Sandstone Formation in relation to global, North American, and European stratigraphic
nomenclature (modified from Falcon-Lang et al. 2011a).
194 H.J. FALCON-LANG ET AL. P A L A I O S
oriented serial sections exist. Unfortunately, hand specimens are not
preserved, so additional investigations cannot be made.
Museum Collections
The thin sections studied here are in the collections of the Bristol City
Museum and Art Gallery (BCMAG: Cc. 5194–5209); the National
Museum and Galleries of Wales, Cardiff (NMGW: 28.3.G17, G19, G21,
G23–G27, G31, G33–G40; G47–G48, G52, G55–G56, G260;
2011.19.G1–4); the British Geological Survey, Keyworth (BGS: MPK
14123–14159; PF 7394, 7400, 7402, 7413–7414, 7416, 7424–7427; PB 309 –
318, 604; RC 1–6, 17–18, 41, 47); and the British Museum of Natural
History, London (BMNH: J.P. 405–406, 827; V. 537, V. 673abc, V.
674ab, V.5237E1–2; V. 5237(19, 20, F, G), V. 5875abc, V. 8906–8930, V.
9911–9912, V. 51430, V. 51543); all in the UK.
Plant Biology and Ecology
Of the , 72 separate plant specimens represented, 62 (87%) are
cordaitaleans (44 Dadoxylon, 11 Mesoxylon, 7 Amyelon), five (7%) are
marattialean tree ferns (Psaronius trunks), two are lycopsids (2.5%), two
are sphenopsids (2.5%), and one is a pteridosperm (1%) (see Falcon-Lang
et al. 2012 for a full systematic description of this assemblage). One
additional specimen (not described in Falcon-Lang et al. 2012) is not a
plant fragment but comprises a large, solitary coprolite.
Plant–arthropod associations are observed only in the cordaitalean
and tree-fern axes. Cordaitaleans were woody gymnosperms with varied
growth forms (Rothwell 1988), but the type found in the Pennant
Sandstone Formation is inferred to have been a large tree with a
substantial trunk of pycnoxylic, Dadoxylon-type wood (Falcon-Lang
and Bashforth 2004, 2005), deeply penetrative roots of Amyelon type,
and juvenile axes (mostly branches) of Mesoxylon type bearing
evergreen leaves (Falcon-Lang et al. 2011a, 2012). The marattialean
tree fern, Psaronius, was characterized by a buttressing skirt of
subaerial adventitious roots, composed of a compact inner root mantle
and an outer root mantle of larger-diameter, aerenchymatous free
rootlets (Morgan 1959; Ehret and Phillips 1977; DiMichele and Phillips
1994).
The cordaitalean dominance of this allocthonous permineralized
assemblage differs markedly from pteridophyte-dominated megaflora
and palynoflora assemblages, obtained from coals and gray roof shales
(coal swamps) that intermittently occur between the channel sandstone
bodies of the Pennant Sandstone Formation (Pendleton et al. 2012).
Based on the widespread development of weakly developed growth
interruptions in the cordaitalean woods (cf. Falcon-Lang et al. 2011b),
preservation as calcareous permineralizations (Matysova´ et al. 2010), and
taphonomic and sequence stratigraphic considerations (Falcon-Lang et
al. 2012), this distinctive allochthonous channel-lag assemblage is
interpreted as remains of a better-drained ecosystem that grew in riparian
environments, probably under somewhat drier (subhumid) climatic
conditions (Falcon-Lang et al. 2011a, 2012) than those prevalent in the
coeval coal swamps.
Methods
In our study of plant–arthropod associations, material was examined
and imaged using an Olympus binocular BH-5 microscope with a Nikon
digital camera system and software. Qualitative descriptions of associa-
tions in transverse (TS), radial longitudinal (RLS), and tangential
longitudinal (TLS) sections were supplemented, in some cases, with
quantitative analysis of microcoprolite and tunnel diameter data. The
short and long axis of microcoprolites was measured as a proxy for
arthropod instar size. Diameter data were obtained, to the nearest
micron, using the measurement tool in the Nikon software. A population
of up to 400 microcoprolites (the first 400 encountered in the slide, as
measured from a random point), and all available tunnels, were measured
for each specimen.
INSECT HERBIVORE ASSOCIATION
Wound Response in a Mesoxylon Branch (Type 1)
Description.—This plant–arthropod association is only seen in two of
eleven (18%) cordaitalean axes of Mesoxylon type (BGS PB 312–318;
BCMAG Cc. 5194–5196). The following description is based solely on the
BGS sections, which comprise multiple sections through the same axis,
and most clearly illustrate the association.
Viewed in seven serial TS sections, cut over a longitudinal distance of
14 mm, the BGS axis is slightly flattened, comprising a pith area, 3.5 3
6 mm diameter, surrounded by a radius of secondary xylem, 3.1–4.6 mm
wide (Fig. 3A). Four growth interruptions (1–4) are seen in the secondary
xylem (Fig. 3B). Leaf traces, originating from protoxylem bundles
adjacent to the pith, persist to the outer preserved edge of the axis
(Fig. 3A–C). No extraxylary tissue is preserved.
A prominent feature seen in all seven serial sections is a wound,
encompassing up to 30% of the circumference of the axis. The wound
involves the excavation of the cambium, secondary xylem, and
presumably extraxylary tissue (although this is nowhere preserved), as
well as the entire contents of the pith assuming that parenchyma was
present earlier (Fig. 3A, B). Only the outermost pith cells adjacent to the
primary vasculature have survived (Fig. 3B).
Later-formed traumatic secondary xylem (postdating the wound)
wraps round the truncated surface, infilling the excavation and most
of the innermost pith space (Fig. 3C). It preserves some relicts of the
cambial zone and periderm where it spills into the former pith area
(Fig. 3B). Wound reaction tissue consists of bulbous tuftlike regions,
composed of hyperplasic, and occasionally hypertrophic, files of
secondary xylem tissue (Fig. 3C). Based on the radius of the zone
between the secondary xylem formed before and after the wound,
damage was incurred when the secondary xylem was 0.3 mm thick,
coinciding with the growth interruption 1 in the wood (Fig. 3B, C).
The outer surface was entirely healed when the secondary xylem
layer was 1.2 mm thick, coincident with growth interruption 4
(Fig. 3B).
Running the entire observed length (14 mm) of the former pith area,
there is an open chamber, 0.98–1.64 mm diameter (Fig. 3A, B). This
contains a few spheroidal macrocoprolites (310–708 mm diameter, mean:
616 mm, n 5 6) composed mostly of equant thin-walled parenchyma
(probably pith cells), equant thick-walled sclerenchyma (possibly pith or
periderm cells), and a few elongate tracheids derived from the xylem
(Fig. 3D).
Interpretation.—The association consists of damage to cordaitalean
branches resulting from the near-complete consumption of a narrow
radial segment of cambial tissue and nearby xylem and pith. The
thickness of the secondary xylem predating the trauma (0.3 mm) shows
that the wound was made to a young leafy shoot, probably less than 1 year
old, and reaction tissue further demonstrates that the shoot was alive.
Hence, the tracemaker is inferred to have been herbivorous. If growth
interruptions were caused by tropical rainfall fluctuations, the leafy
branch may have been stripped during the dry season; however,
conversely, the interruptions could have been directly induced as wound
response. The contents of macrocoprolites suggest that pith parenchyma
cells were the primary target of feeding, with a few tracheids probably
ingested incidentally. Based on the relatively large diameter of the
macrocoprolites (, 0.3–0.7 mm), and the clear evidence for herbivory, the
tracemaker was, probably, an insect (Labandeira and Phillips 2002).
PENNSYLVANIAN PLANT–ARTHROPOD ASSOCIATIONS IN SOUTHERN BRITAIN 195P A L A I O S
ORBATID MITE DETRIVORE ASSOCIATIONS
Microcoprolite-Filled Galleries in Psaronius Root Mantle (Type 2a)
Description.—This association occurs in the inner root mantle of two of
five (40%; BCMAG Cc. 5206, 5208) specimens of a Psaronius cf. blicklei
marattialean tree fern. In these specimens, the inner root mantle comprises
vertically oriented rootlets, 1–3 mm diameter, embedded in a parenchy-
matous interstitial tissue. Individual rootlets consist of an exarch stellate
actinostele of scalariform-thickened tracheids, 70–200 mm diameter,
surrounded by an aerenchymatous cortex containing elongate air chambers
(lumina), enclosed within an outer layer of sclerenchyma (Fig. 4A).
The plant–arthropod association comprises spheroidal to slightly
ovoidal microcoprolites (length/width ratio 1.16; Table 1), located within
long tunnels excavated along cortical lumina (and adjacent tissues) of
rootlets, but not in surrounding interstitial tissue (Fig. 4B, C). The
tunnels, 120–410 mm in diameter (mean 238 mm, n 5 67) are circular in
cross section (Fig. 4A), but locally expand into irregular galleries (up to
1.5 mm wide), approximately paralleling the general rootlet axis
(Fig. 4B). In several cases, the rootlet actinostele has been displaced to
the edge of the rootlet to accommodate the largest galleries (Fig. 4B).
Microcoprolites, 15–97 mm in diameter, are packed in elongate clusters
that occupy much of the width of tunnels and galleries, and are separated
from adjacent clusters by narrower trails of a few microcoprolites (Fig. 4C).
Some microcoprolites are deposited within scalloped hollows excavated
into the parenchymatous edge of the cortex (Fig. 4D). In general, the
coprolites occur as size-sorted populations, with four or five distinct size
classes represented (see data below; three size classes illustrated in Fig. 4E).
Interpretation.—This association of microcoprolites occurring in
rootlet lumens and adjacent tissues of Psaronius root mantle has been
FIG. 3.—Type 1 association: Herbivore cambial wound response and macrocoprolites in cordaitalean (Mesoxylon cf. sutcliffii) branches. A) Branch showing wound,
where cambial tissue, xylem, and pith have been consumed, prior to subsequent healing by traumatic xylem; TS, BGS PB 312, scale bar 5 2 mm. B) Interpreted sketch of
branch in view A showing that wound (demarked by the two arrows) was incurred shortly after growth interruption 1 and had not fully healed until growth interruption
4; TS, based on BGS PB 312, scale bar 5 2 mm. C) Enlargement of boxed area in view A (but in adjacent serial section) showing damaged edge of secondary xylem (solid
line, ts) and pith (dotted line), which occurred at the time of growth interruption 1. Prior to growth interruption 2, growth of traumatic secondary xylem had partly healed
the wound; TS, BGS PB 313, scale bar 5 600 mm. D) Enlargement of macrocoprolite from central chamber, but seen in a different serial section than that in view A.
Contents mostly include parenchyma, sclerenchyma with some partially digested tracheids; TS, BGS PB 315, scale bar 5 200 mm. Abbreviations: c 5 macrocoprolite; ch
5 chamber; htx 5 xylem with hyperplasic and hypertrophic tracheids; lt 5 leaf trace; pi 5 pith parenchyma (pale blue in B); pr 5 periderm (purple in B); px 5 primary
xylem poles (circles); sx 5 normal secondary xylem (orange in B); tr 5 tracheids; ts 5 truncation surface along wound; tx 5 traumatic secondary xylem (pink in B); 1–4 5
successive growth interruptions.
196 H.J. FALCON-LANG ET AL. P A L A I O S
well documented, principally, from Late Pennsylvanian coal-ball floras
such as the Calhoun Coal of the eastern United States, where it is has
been interpreted as the activity of oribatid mites (Labandeira et al. 1997a;
Labandeira 2001). The rise of this arthropod association parallels the
spectacular emergence and dominance of marattialean tree ferns after the
demise of most elements of the coal-swamp flora, including cordaitaleans,
near the Middle to Late Pennsylvanian boundary (Phillips et al. 1974).
Notably, the association of rootlet detritivores with Psaronius is virtually
FIG. 4.—Type 2a association of detritivore microcoprolites occurring with marattialean (Psaronius cf. blicklei) root-mantle tissues. A) Inner root mantle showing
tunnels (5 t, and dotted circles and arrow), which are generally circular to subcircular in cross section. TS, BCMAG Cc. 5206, scale bar 5 2 mm. B) Enlargement of root
and associated tissues, showing clustered distribution of microcoprolites within a longitudinal gallery positioned between the inner root actinostele (displaced) and outer
wall of sclerenchyma. TS, BCMAG Cc. 5206, scale bar 5 750 mm. C) Clusters of microcoprolites deployed along a longitudinal tunnel within the root cortex. LS,
BCMAG Cc. 5208, scale bar 5 500 mm. D) Unimodal microcoprolites within scallop hollow excavated into aerenchymatous tissue, along an inner root surface. LS,
BCMAG Cc. 5208, scale bar 5 300 mm. E) Multi-modal size distribution of small (1), medium (2) and large (3) microcoprolites adjacent to a scalariform-thickened
tracheid. LS, BCMAG Cc. 5208, scale bar 5 200 mm. Abbreviations: as 5 actinostele; c 5 cortex; cp 5 cortical parenchyma; it 5 interstitial tissue; mc 5 microcoprolite;
mcg 5 microcoprolite-filled gallery; s 5 sclerenchyma; t 5 longitudinal tunnel (also highlighted by dotted circles); 1–3 5 microcoprolite size classes from small to large.
TABLE 1.—Oribatid microcoprolite size data. Abbreviations: Sd, Standard deviation; L/S, ratio of the long and short axes.
Specimen Taxon
Long (L) axis (mm) Short (S) axis (mm)
L/S ratioMean 6 Sd Range Mean 6 Sd Range
BGS PF 7424 Dadoxylon 69.35 6 20.20 27–122 53.35 6 15.70 26–92 1.30
BGS MPK 14144 Mesoxylon 61.68 6 20.21 17–128 47.81 6 18.10 15–93 1.29
BGS PF 7425 Dadoxylon 65.33 6 19.27 25–125 50.78 6 14.37 20–89 1.29
BGS PF 7427 Dadoxylon 74.59 6 17.11 22–130 58.52 6 13.37 22–93 1.27
NMGW 28.3.G52 Dadoxylon 42.37 6 9.86 18–75 32.17 6 6.98 15–52 1.31
BMNH V. 8909 Dadoxylon 44.05 6 12.97 14–79 31.47 6 8.74 14–57 1.39
BMNH V. 8910 Dadoxylon 50.38 6 16.03 17–106 36.14 6 11.35 12–73 1.39
BCMAG Cc 5206 Psaronius 52.65 6 18.54 17–97 45.39 6 17.79 15–92 1.16
PENNSYLVANIAN PLANT–ARTHROPOD ASSOCIATIONS IN SOUTHERN BRITAIN 197P A L A I O S
198 H.J. FALCON-LANG ET AL. P A L A I O S
nonexistent in earlier, Middle Pennsylvanian floras. For the Calhoun
flora, it occurs overwhelmingly on P. chasei (Labandeira et al. 1997a;
Labandeira 1998), and less so on rarer P. cf. blicklei, P. magnificus, and a
fourth, unidentified species. Data indicate that this stereotypical
consumption of softer tissues along rootlets of the inner root mantle
persisted for approximately eight million years in Euramerica, minimally
from the early Moscovian (mid-Westphalian) to the mid-Kasimovian
(mid-Stephanian) and into earliest Permian (Ro¨ßler 2000); however, this
type of oribatid microcoprolite association has not been documented on
younger Psaronius material from the Late Permian China (D’Rozario et
al. 2011). As such the early Middle Pennsylvanian (early Moscovian)
association, reported here from the Pennant Sandstone Formation, is one
of the earliest known, widespread occurrences of an oribatid mite
association with Psaronius.
Microcoprolite-Filled Galleries in Dadoxylon Cordaitalean Wood
(Type 2b)
Description.—This association comprises extensive and widespread
tunnels, chambers, and galleries in 16 out of 44 (34%) specimens of
Dadoxylon-type cordaitalean trunk wood (BMNH V. 5875c, 8910; BGS
PB 309, 311, PF 7397–7399, 7400, 7402, 7416, 7424–7425, 7427; NMGW
28.3.G52).
In its simplest form, it comprises predominantly longitudinal to near-
longitudinal tunnels (i.e., oriented parallel to the general xylary grain),
58–454 mm diameter (mean: 197 mm, n 5 72), which are rarely empty
(open) or much more commonly densely packed (closed) with ovoid
(length/width ratio: 1.27–1.39) microcoprolites, 14–130 mm diameter
(Fig. 5A–C). Tunnels are straight to slightly curvilinear along their
length, and may course radially or tangentially for short distances,
intersecting with adjacent tunnels to form a weakly anastomosed
network in three dimensions (Fig. 5C). One unusual specimen (BGS
PB 309) displays 16 tunnels, 52–434 mm diameter, which are circular in
cross section, entirely devoid of microcoprolites (empty), deployed into
four, or probably, five distinct size categories of tunnel width, oriented
tangentially (Fig. 5D; see data below).
Other more complex associations comprise comparatively massive
galleries, 1–3 mm wide and .25 mm long, developed parallel to the
general xylary grain, and consisting of an apparent amalgamation of
smaller tunnels and chambers (Fig. 5E, F), densely packed with
microcoprolites (Fig. 5G). Individual microcoprolite-filled tunnels are
of similar dimensions (96–411 mm) to those reported in simpler
associations, and late-stage tunnels and associated chambers may be
empty (open) and truncate earlier microcoprolite-filled excavations
(Fig. 5E, G). Within galleries, microcoprolites may be, locally, clustered
in areas that are circular in cross section with extremely dense
arrangements, possibly representing the position of former tunnels that
were subsequently closed (Fig. 5F). Individual galleries are separated by
curved, flaplike partitions of apparently more resistant xylary tissue
(Fig. 5E). Galleries are often developed along zones of postmortem
weakness (cracks), which may also contain silt to very fine sand-grade
quartz sediment.
Interpretation.—This association is identical to previously reported
material attributed to oribatid mites in cordaitalean wood (Labandeira et
al. 1997a). The earliest, abundant occurrence of such an association in
cordaitalean secondary xylem (Dadoxylon protopityoiodes Felix) of
Euramerica is from the lowermost Pennsylvanian of the Upper Silesian
Coal Basin in southern Poland (Brzyski 1969). However, the most
extensive documentation of this association has been from coal-ball floras
of at least eight overwhelmingly Middle Pennsylvanian deposits in the
Illinois and Appalachian Basins of the eastern United States (Cichan and
Taylor 1982; Scott and Taylor 1983; Labandeira et al. 1997a). The same
style of borings with densely packed microcoprolites also have been found
in Middle Pennsylvanian localities from the Midcontinent of the United
States, principally in coal-ball deposits in Iowa and Kansas (Baxendale
1979; Raymond et al. 2001), where some cordaitalean taxa arguably had
mangrove-like habits (Raymond et al. 2010). Oribatid mite borings in
cordaitalean wood are the most pervasive plant–arthropod association of
the Middle Pennsylvanian of Euramerica, and represent the extensive,
apparently efficient, recycling of decomposing plant material by oribatid
mite detritivores, perhaps trophically analogous to modern termites in
similar lowland, equatorial ecosystems (Raymond et al. 2001). Both
groups also play an essential role in soil aeration and water retention
(Bardgett 2005).
The unusual association, reported here, of tangentially oriented
tunnels devoid of microcoprolites in BGS PB 309 (Fig. 5D), but of
similar dimensions to those containing microcoprolites, is worthy of
further comment. These elongate, subparallel tunnels have smooth,
confluent borders where individual xylem cells have been snipped with
precision, again, presumably by the mouthparts of an oribatid mite.
Reasons for the curious absence of microcoprolites in these arthropod
borings could include: (1) the original fecal pellets were subsequently
washed out of the tunnels during fluvial transport, or (2) clusters of
solid, particulate excreta were produced only occasionally within
tunnels at intervals that would not be recorded within all sections. A
search of the Paleozoic literature revealed only one similar example, a
specimen of Ankyropteris corrugata root from the Pennsylvanian-age
Coal Measures of the UK, showing a coprolite-free region surrounded
by a wound response (Holden 1906); however, this specimen indicates
herbivory, and differs from the association reported here (Fig. 5D). The
reason for the paucity of microcoprolite-free tunnels in the primary
literature probably is due to the fact that the presence of micro-
coprolites is often used as essential evidence for an arthropod
fabricator. Although in cross section many forms of fungal decay such
as white pocket rot closely resemble the arthropod tunnels described
here (Weaver et al. 1997), multimodality in tunnel size makes this
alternative interpretation unlikely.
r
FIG. 5.—Type 2b association of detritivore microcoprolite-laden galleries and tunnels in cordaitalean (Dadoxylon sp.) trunk wood. A) Longitudinal tunnel densely
packed with microcoprolites. RLS, BGS PF 7427, scale bar 5 300 mm. B) Tunnel with circular cross section densely packed with microcoprolites. TS, BMNH V. 8909,
scale bar 5 250 mm. C) General view of longitudinally, radially, and tangentially oriented tunnels (highlighted) suggestive of a weakly anastomosed pattern. RLS, BMNH
V, 8909, scale bar 5 1 mm. D) Open (empty) tunnels occurring as five distinct size classes (only size classes 1, 2, and 5 are illustrated; size classes 3 and 4 are observed
elsewhere in the same section). RLS, BGS PB 309, scale bar 5 500 mm. E) Substantial microcoprolite-filled galleries comprising multiple amalgamated closed chambers
(right-hand example is highlighted to show morphology). Networks of open tunnels and chambers truncate earlier galleries. RLS, BGS PF 7427, scale bar 5 750 mm. F)
Enlarged view of microcoprolite-filled gallery shown in view E showing very densely packed clusters of microcoprolites that might mark positions of former tunnels. RLS,
BGS PF 7427, scale bar 5 200 mm. G) Enlarged view of open chamber shown in view E showing truncation (coprophagy) of earlier-deposited microcoprolite-filled
gallery. RLS, BGS PF 7427, scale bar 5 250 mm. Abbreviations: ch 5 chamber filled with microcoprolites; ct 5 closed tunnel filled with microcoprolites; mcg 5
microcoprolite-filled gallery; och 5 open chamber; ot 5 open tunnel.
PENNSYLVANIAN PLANT–ARTHROPOD ASSOCIATIONS IN SOUTHERN BRITAIN 199P A L A I O S
Microcoprolite-Filled Galleries in a Mesoxylon Cordaitalean Branch
(Type 2c)
Description.—This association is seen in a single Mesoxylon axis (BGS
MPK 14144) which shows, in transverse section, a network of relatively
large,, 0.5–1.5 mm wide tunnels with internal loops, cul-de-sacs, branches,
and an overall curvilinear trajectory (Fig. 6A, B) filled with dark
amorphous matter and quartz-rich sediment (Fig. 6C). While these tunnels
also contain, locally, zones of densely packed microcoprolites, 17–128 mm
diameter (Fig. 6C), most microcoprolite material is deployed in galleries,
chambers, and smaller-scale tunnels developed adjacent to the main
conduits (Fig. 6D). The main tunnel system meanders from one or two
possible entry points at the outer edge of the axis, through several loops,
before entering the pith region, where further microcoprolites are deposited
(Fig. 6A, B). As seen in Dadoxylon specimens, circular areas of extremely
densely arranged microcoprolites probably represent the former position of
closed tunnels, while late-stage tunnels remain open (empty) (Fig. 6D).
Interpretation.—This association is very similar to Type 2b reported
above and is attributed to oribatid mites (Labandeira et al. 1997a). The
unusual meandering geometry of the gallery network, in contrast to the
predominantly linear and longitudinal network in Dadoxylon, probably
reflects the mites tracking concentric and radial lines of weakness in this
small-diametered axis rather than any significant difference in behavior.
Oribatid Mite Instars Deduced from Microcoprolite Diameters
Description.—The long and short axis of microcoprolites was measured
for large populations (n 5 400 per specimen) in Dadoxylon and Mesoxylon
specimens, and quantitatively analyzed to shed further light on oribatid
ontogeny. Placed into 1-mm-continuous-size bins (0–1, 1–2, etc.), data were
plotted as a frequency histogram, and the noise muted by plotting a 5-point
moving average (Fig. 7, overlain black line). This data expression revealed
typically four or five microcoprolite size modes for each specimen, with
step ratios that steadily decline (Table 2). For example, in MPK14144
(Fig. 7), modes occur at 33, 52, 74, and 100 mm (the subdued peak at 83 mm
is probably artifactual), and successive step ratios are 1.58, 1.42, and 1.35.
Too few microcoprolites could be measured to perform similar analyses for
Psaronius specimens; however, qualitative observations suggest four or five
modes for this material as well.
Interpretation.—Microcoprolite size multimodality is clearly a signif-
icant feature of these fossil populations. We further note that numerous
clusters of oribatid mite microcoprolites occur within elongate tunnels in
FIG. 6.—Type 2b association of detritivore microcoprolite-laden tunnels and galleries in cordaitalean branch (Mesoxylon sp.). All images from BGS MPK 14144. A)
Cross section of Mesoxylon axis showing a network of , 0.5–1.5-mm-wide tunnels with internal loops, cul-de-sacs, and an overall curvilinear trajectory filled with dark
amorphous matter, quartz-rich sediment, and distinctive microcoprolites; some adjacent areas comprise microcoprolite-laden galleries. TS, scale bar 5 3 mm. B)
Interpreted sketch of structures seen in view A; pale gray 5 secondary xylem; medium gray 5 major tunnel system; dark gray 5 microcoprolite-filled chambers, galleries
and tunnels. TS, scale bar 5 3 mm. C) Enlarged view of part of specimen in view A highlighting looping tunnels filled with clastic quartz sediment, with adjacent
microcoprolite-laden galleries. TS, scale bar 5 500 mm. D) Enlarged view of one microcoprolite-laden gallery, highlighting open (empty) tunnels and closed
microcoprolite-filled tunnels. TS, scale bar 5 400 mm. Abbreviations: cs 5 clastic sediment; ct 5 closed microcoprolite-filled tunnel; g 5 gallery; mcg 5 microcoprolite-
filled gallery; ot 5 open tunnel; pi 5 pith; sx 5 secondary xylem.
200 H.J. FALCON-LANG ET AL. P A L A I O S
TABLE 2.—Analysis of multimodality in oribatid microcoprolite size data. Step-ratios are the ratios of successive modes.
Specimen Taxon Number of modes Modes (mm) Step ratios Mean step ratio
BGS PF 7424 Dadoxylon 4 44, 61, 83, 109 1.39, 1.36, 1.31 1.35
BGS MPK 14144 Mesoxylon 4 33, 52, 74, 100 1.58, 1.42, 1.35 1.45
BGS PF 7425 Dadoxylon 4 36, 50, 68?, 91? 1.38, 1.36, 1.33 1.36
BGS PF 7427 Dadoxylon 4 54, 69, 86?, 102 1.27, 1.24, 1.18 1.24
NMGW 28.3.G52 Dadoxylon 5 24, 34, 44, 55, 66 1.41, 1.29, 1.25, 1.20 1.29
BMNH V. 8909 Dadoxylon 5 26, 33, 42, 53, 64 1.27, 1.27, 1.26, 1.21 1.25
BMNH V. 8910 Dadoxylon 5 33, 43, 53, 64, 75 1.30, 1.23, 1.21, 1.17 1.23
BCMAG Cc 5206 Psaronius n/d n/d n/d n/d
FIG. 7.—Frequency–distribution data of long-axis microcoprolite lengths placed into 5 mm bins (based on 400 measurements from BGS MPK 14144). Data are
multimodal with peaks at 33, 52, 74, and 100 mm and mean step ratio of 1.45. The subdued mode at 83 is inferred to be a data artifact.
PENNSYLVANIAN PLANT–ARTHROPOD ASSOCIATIONS IN SOUTHERN BRITAIN 201P A L A I O S
the fossil material, and individual clusters of microcoprolites appear, as in
modern networks (Drift 1964), with each cluster consisting of micro-
coprolites of near-identical size. The microcoprolites often are grada-
tionally arrayed along a tunnel from smaller clusters with smaller-sized
fecal pellets to larger clusters with larger-sized fecal pellets (Kubiena
1955). The quantitative data collected here therefore provide an
opportunity to assess whether size multimodality and size clustering
reflect instar-to-instar developmental size increases.
Oribatid mites are members of the morphologically distinct clade,
Cryptostigmata (Norton 1994), and almost always exhibit a develop-
mental sequence of five active feeding instars (Norton and Ermilov 2014),
separated by a very a brief molt interval. After hatching from the egg,
which includes the nonfeeding prelarva, the five active instars are: larva
R protonymph R deutonymph R tritonymph R adult. Linear
dimensions of body sclerites and fecal pellets scale the same for each
posteclosion instar, gleaned from intraspecific populations (Saichuae et
al. 1972; Ermilov et al. 2011; Norton and Ermilov 2014), or at the coarser
level of congeneric species (Walter and Proctor 1999). Applying this
understanding to the fossil material, the expectation would be for five
modes, reflecting the five posteclosion instars. While five modes are seen
in some specimens, others show only four modes, as in MPK14144
(Fig. 7), where modes occur at 33, 52, 74, and 100 mm. Nevertheless, in
modern oribatid mites the first, posthatching, active instar, the larva,
typically is miniscule and defecates among the smallest of detectible fecal
pellets. Consequently, extending the small detectible mode at 33 mm
backward, by inferred step-change values, would imply a mode at about
16 mm, which coincides exactly with the smallest observed microcoprolite
size class. Alternatively, the last peak could include pellets from both
tritonymph and adult stages, as they are approximately of the same size,
and in some oribatid genera the tritonymph is absent. Accepting any one
of these explanations, quantitative documentation of microcoprolite
multimodality, and indeed, qualitative observations on tunnel multi-
modality, both of which display four or five modes, is consistent with
oribatid mite instar development.
Microcoprolite allometry of fossil material also shows remarkable
parallels with that of modern mites. Excluding the largest (1.58) and
smallest (1.17) outliers, microcoprolite populations show modal step
ratios of 1.20–1.41 (Table 2). Similarly, modern mites exhibit step ratios
averaged between all adjacent instar pairs in the range of 1.20–1.41, or
slightly more than the square root of 2, which scales with a doubling of
mass between consecutive instars (Walter and Proctor 1999; also see
Przibram and Megusˇar 1912). This central tendency of modal values is
the same for the much larger hemimetabolous insects (Cole 1980).
Another noteworthy aspect of the fossil data is that the second mode (for
populations with four modes) or the third mode (five modes) is usually
dominant. In modern oribatid mite biology, the dominant feeding phase
begins with the protonymph and peaks with the deutonymph (Shereef
1976; Norton and Ermilov 2014). By contrast, the last instar, the adult,
also foreshadowed somewhat by the tritonymph, is characterized by a
significant diminution of growth rate expressed in the growth ratio. This
decrease represents the shift from a feeding to a reproductive phase of the
mite life cycle; the fossil data reported here appear to reveal a similar
pattern. Remarkably, Middle Pennsylvanian oribatid mites, separated
by ca. 311 myr of evolutionary biology, apparently had a similar
developmental biology to modern counterparts.
PUTATIVE ARTHROPLEURID ASSOCIATION
Very Large Solitary Coprolite (Type 3)
Description.—This association comprises a solitary, subrounded
macrocoprolite (NMGW 28.3.G42) of very considerable size. The
macrocoprolite has an incomplete long axis of 19 mm and an incomplete
short axis of 14 mm; however, prior to mechanical breakage during
transport in the bedload of braided river channels, the original
dimensions were, probably, even larger (Fig. 8A). The macrocoprolite
is composed of two components, the relative proportions of which were
quantified using an eye-piece-mounted graticule. Most abundant are
ragged fragments of vascular plant tissue, 0.4–2.1 mm long, and a few
spores, which together comprise a loose, somewhat interwoven frame-
work (Fig. 8A); individual fragments showing every stage of decay, from
excellent subcellular preservation to near-structureless material (44%;
Fig. 8B, C, E). Of the few plant fragments that retain anatomy, most
show scalariform-thickened tracheids with localized fimbrils between bars
(Fig. 8B), while a few others are thick tracheids showing 5- to 7-seriate
alternate pitting, lacking prominent borders (Fig. 8C). The other
component comprises subrounded, silt-sized (typically 5–50 mm diameter)
fragments of micritic carbonate and quartz (38%), which are randomly
distributed through the organic framework (Fig. 8A, D). The remaining
cross-sectional area (18%) of the macrocoprolite comprises randomly
distributed pore spaces, typically 3–22 mm diameter, which remain
permanently black when rotated in cross-polar illumination (Fig. 8A).
The macrocoprolite also contains two conspicuous oval burrowlike
structures, which are near-identical in size and shape (89 3 53 mm and 87
3 50 mm), and show a distinct 4-mm-thick lining (Fig. 8D). A dark,
cryptic segmented feature is also seen (Fig. 8F).
Interpretation.—This is one of the largest, if not the largest, coprolite
ever documented from Pennsylvanian strata (at least 19 3 14 mm),
significantly larger than the 3.5 mm coprolite described by Labandeira
et al. (1997) from the Middle Pennsylvanian (Moscovian) of Illinois,
United States. Coprolite size is, very broadly, proportional to the body
size of the animal that produced it, so we infer that the producer was in
the decimeter to meter size range. We also infer that the coprolite
producer was terrestrial because of the macrocoprolite’s fluvial context
and calcified state, suggesting that it was mineralized in a well-drained
soil. There were only two groups of terrestrial Pennsylvanian animal that
could have produced a macrocoprolite of this size: tetrapods and giant
arthropods. Sahney et al. (2010) synthesized literature on the dentition
and postcranial anatomy of Pennsylvanian–Permian tetrapods to infer
diet, and suggested that tetrapod herbivory did not evolve until the
Kasimovian, ca. eight million years later than our fossil material.
Furthermore, the contents of the coprolite; which contains plant material
showing a wide range of decay states, mostly derived from trunk wood,
coupled with the high sediment content; is more consistent with a
detritivorous feeding habit rather than herbivory (Labandeira 1998).
These considerations tend to argue against a tetrapod producer, although
this unlikely possibility cannot be ruled out. Of the arthropods, the only
known group of terrestrial Carboniferous detritivores of sufficiently
substantial size to have produced our coprolite were the arthropleurids
(Shear and Edgecombe 2010), the larger forms of which have a Mid-
Mississippian (early Visean) to earliest Permian (Asselian) range (Martino
and Greb 2006). Although arthropleurids originated in the Devonian,
body fossils (Wilson and Shear 1999) and possible aestivation burrows
(Morrissey and Braddy 2004; Morrissey et al. 2012) are of considerably
smaller size than their later Paleozoic descendants.
Identifiable plant fragments seen in the macrocoprolite mostly
comprise lycopsid wood (Cichan and Taylor 1982; Fig. 8B) and other
tissues suggestive of calamiteans or medullosans (DiMichele and Phillips
1994; Fig. 8C). This composition suggests that these plants may have
formed a significant component of the arthropleurid diet, consistent with
earlier interpretations (Rolfe 1985). Apparently mucous-lined burrows
(Fig. 8A, D) within the macrocoprolite imply that possible arthropleurid
fecal material was processed by smaller invertebrates, possibly oligo-
chaete annelids. The cryptic segmented feature seen in the macrocoprolite
may represent a body fossil of one such annelid (Fig. 8F). Of course,
202 H.J. FALCON-LANG ET AL. P A L A I O S
attribution of the macrocoprolite to arthropleurids is not absolutely
certain, however, because other large terrestrial detritivores may have
existed for which there is currently no fossil record (cf. Fayers et al. 2010).
DISCUSSION
The plant–arthropod associations described here are significantly
diverse for their Middle Pennsylvanian age, and are noteworthy in that
they represent a rare snapshot of interactions in subhumid tropical
environments outside the relatively well-sampled coal swamps (DiMichele
and Phillips 1994; DiMichele et al. 2007). It is likely that a taphonomic
megabias exists in the fossil record of arthropod associations similar to
that recently documented for plant communities (Falcon-Lang et al. 2009,
2011). However, the three associations documented here are also
significant in their own right as outlined below:
Insect Herbivory (Type 1)
The intriguing herbivorous association of a large arthropod, most
likely an insect, in two cordaitalean stems provides an example of how
typical detritivory could be transformed into incipient and subsequent
full-fledged herbivory. A close analogue to the cordaitalean example
involves Psaronius trees, for which greater detail exists regarding pith
borings and the distribution of live versus dead tissues within the
ontogeny of the plant (Mickle 1984; Ro¨ßler, 2000). Standing P. blicklei
and P. chasei trees evidently exhibited trunk necroses caused by fungal
heartrot at levels closer to ground level while the same plants
simultaneously bore live trunk and photosynthetic frond tissues toward
their canopies (Mickle, 1984; Roßler, 2000). Maintenance of tree support
would have been assumed by production of structural, buttressing tissues
of inner root mantle that anchored the plant basally (Roßler, 2000). For
pith borers consuming decaying parenchymatic tissues at the lower trunk
regions in P. blicklei, P. chasei, P. ‘‘layered cells’’ morphotype, P.
magnificus, and P. housuoensis (Rothwell and Scott, 1983; Roßler 2000;
Labandeira and Phillips 2002; D’Rozario et al. 2011), there was a larval
or adult insect progressing vertically upward, eventually encountering live
tissues adjacent to the upper trunk reaches near the canopy (Labandeira
and Phillips 2002). Feeding encounters on live parenchymatic, especially
meristematic tissues, would elicit tissue response, such as production of
tufts of hypertrophic and hyperplasic tissue, or callus, similar to that seen
in the two cordaitalean specimens described herein. Histological
FIG. 8.—Type 3 association of very large (19 3 14 mm) coprolite comprising meshwork of mostly vascular plant fragments, together with spores and clay/silt-grade
sediment. All images from NMGW 28.3.G42. A) General view of coprolite highlighting two lined tunnels (arrows), scale bar 5 2.5 mm. B) Tracheids showing
scalariform-thickening with microfibrils, scale bar 5 100 mm. C) Tracheids showing multiseriate, alternate pits, scale bar 5 50 mm. D) Expanded view of one of the lined
tunnels shown in view A, scale bar 5 750 mm. E) Probable partially digested spore, scale bar 5 250 mm. F) Detail of cryptic segmented feature, scale bar 5 300 mm.
PENNSYLVANIAN PLANT–ARTHROPOD ASSOCIATIONS IN SOUTHERN BRITAIN 203P A L A I O S
refinements of this interaction between an insect pith borer and Psaronius
trunk parenchyma could have resulted in a primitive gall association,
wherein response tissue is subtly modified into inner nutritive tissue for
the gall chamber occupant, and outer structural tissue is designed to
provide protection. Transformations of pith borings to stem galls have
been demonstrated in anthomiid flies (Gassmann and Shorthouse 1992)
and weevils (Shorthouse and Lalonde 1986). Accordingly, primitive galls
have been found as host-plant and tissue specialists in P. chasei frond
petioles from the Late Pennsylvanian Calhoun Coal (Labandeira and
Phillips 1996b).
Oribatid Mite Detritivory (Type 2)
Mite associations reported here document a major web of detritivory
on cordaitalean and Psaronius tissues that now extends biogeographically
to eastern Euramerica. Formerly, this mid-Moscovian, few-million-year-
long pulse of detritivory, centered on ca. 311 Ma, was documented in
three regions of eastern North America—isolated midcontinental basins
of principally Iowa and Kansas, the Illinois Basin centered in south-
central Illinois, and the Appalachian Region consisting of the Northern,
Central, and Southern Appalachian Basins (Baxendale 1979; Cichan and
Taylor 1982; Labandeira et al. 1997a; Raymond et al. 2001). It should not
be surprising that eastern Euramerica, along the Variscan Deformation
Front of the southern United Kingdom, should also exhibit the same
nexus of plant hosts and arthropod detritivores and herbivores.
Quantitative aspects of our oribatid microcoprolite analysis extend
previous analysis of holometabolous insect larval coprolites (Labandeira
and Phillips 1996b, 2002), based on Dyar’s Rule and fecal pellet size-
increment relationships in modern insect larvae (Dyar 1890; Sardesai
1969; Cole 1980). We reestablished the importance of applying a
population concept for understanding the biological importance of
coprolites through the use of more robust, discrete statistical data. In the
previous study of macrocoprolites made by galler larvae in Pteridotor-
ichnos stipitopteri petiolar galls, 102 measurements of macrocoprolite
diameters were made, pooled into a single population, which yielded
modal frequency classes from which four larval instars were inferred as
present within the gall. The data indicated an instar ratio range of 1.23–
1.47 (n 5 102), averaging to a mean of 1.33 for all four modes. The
current study of a mite boring involves a similarly endophytic association,
but a near quadrupling of measurements based on macrocoprolite long
axis and short axis dimensions, and recording seven separate micro-
coprolite populations, resulting in four or five modes (depending on the
population) encompassing an instar ratio range of 1.23–1.45 (n 5 402),
and averaging to a grand mean of 1.31. This consistency in replicability of
fossil macrocoprolite data from insect galls and mite borings also is
comparable with fecal-pellet and body-length measurement data from
modern mites (Lebrun 1968; Saichuae et al. 1972; Walter and Norton
1984; Norton and Ermilov 2014).
Putative Arthropleurid Detritivory (Type 3)
Finally, discovery of what is the largest-known terrestrial coprolite of
Pennsylvanian age sheds light on arthropleurid behavior, an iconic but
poorly understood group of arthropods. Identifiable plant remains within
the macrocoprolite support previous conjecture (Rolfe 1985) that
arborescent lycopsids formed an important component of the diet of
these organisms. Documentation of burrows within the macrocoprolite
also provides evidence for two-tiered processing of plant material,
perhaps involving annelids.
ACKNOWLEDGMENTS
HFL gratefully acknowledges receipt of a Natural Environment Research
Council (NERC) Advanced Fellowship (NE/F014120/2) held at Royal
Holloway, University of London. RK acknowledges receipt of a Nuffield
Undergraduate Research Scholarship. This is contribution 234 of the
Evolution of Terrestrial Ecosystems consortium at the National Museum of
Natural History, in Washington, D.C. We thank Roy Norton for assistance
on the modern oribatid mite literature.
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Received 4 September 2014; accepted 28 November 2014.
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