ic
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oprolites in the ground tissue of the permineralized stem of Psaronius housuoensis
coprolites are circular to oval in shape, ranging
Palaeogeography, Palaeoclimatology, Palaeoecology 306 (2011) 127?133
Contents lists available at ScienceDirect
Palaeogeography, Palaeocli
e lsCoprolites (fossilized fecal pellets) have an important role for
understanding plant?insect associations in terrestrial ecosystems of
the deep past. Coprolites, which are attributable to land arthropods
have been identi?ed in sedimentary rocks as old as the Upper Silurian
by Edwards (1996). Younger coprolites from Upper Carboniferous
(Pennsylvanian) compression ?oras were described by Seward
(1935), followed by identi?cations from both compression (typically
shale) and permineralized (mostly coal ball) plant material by Scott
(1977), Baxendale (1979), Rothwell and Scott (1983), Scott and
Taylor (1983), Taylor and Scott (1983), Rex and Galtier (1986) and
Labandeira and Phillips (1996a, 1996b, 2002). Earlier identi?cations
of coprolites in Carboniferous woods reported by Brongniart (1877)
and Williamson (1880) probably are misattributions and require re-
evaluation. By contrast, Scott (1977) and Rothwell and Scott (1983)
microsporophylls and Ptilophyllum leaf cuticles, respectively, both
attributed to small terrestrial tetrapods. Stoval and Strain (1936)
described Paleogene fecal structures, referred to a mammalian origin.
This brief survey of coprolites from the late Palaeozoic to more recent
occurrences clearly indicates that plant?animal associations have an
ancient history, and were relatively abundant in late Paleozoic
deposits, both as generalized detritivory but also as more specialized
and highly varied types of herbivory (Kevan et al., 1975; Scott, 1977;
1980; Scott and Taylor, 1983; Labandeira, 2002; Labandeira and Allen,
2007).
Todate, thePsaronius assemblage of arthropodassociationsprobably
provides the best evidence of a co-associated plant?arthropod system
that the Paleozoic has to offer, comparable tomodern-day source?plant
communities (Southwood, 1973; Lawton, 1976;Hamilton; 1978; Swain,have described a variety of larger sized and
coprolites than previously described for the E
well, smaller, tiny coprolites in coal balls w
and Yochelson (1953, 1962). In the more r
? Corresponding author.
E-mail address: ashalatandc@gmail.com (A. D'Rozar
0031-0182/$ ? see front matter ? 2011 Elsevier B.V. Al
doi:10.1016/j.palaeo.2011.04.009record, Harris (1946, 1956, 1964) and Hill (1976) reported Middle
Jurassic coprolites from the Yorkshire Flora containing caytonialean1. IntroductionReceived in revised form 7 April 2011
Accepted 13 April 2011
Available online 20 April 2011
Keywords:
Coprolites
Psaronius housuoensis
Plant?arthropod association
Late Permian
South China Block
Insectcontain histologically identi?able tracheids, parenchyma, gum sac cells, spores and fungal remains. Several
lines of evidence indicate that this association was detritivorous, represented a pith boring, andwasmade by a
diplopod or more likely an insect. This discovery extends the temporal duration of the food web of Psaronius
plant?arthropod associations from the late Middle Pennsylvanian to now the Late Permian, and extends the
biogeographic range from the equatorial wetlands of the Illinois, Northern Appalachian, and German
Erzgebirge Basins of Euramerica to now the South China Block of Cathaysia. The Psaronius?arthropod?fungi
component community is spatiotemporally the most persistent of documented Paleozoic associations in the
fossil record.
? 2011 Elsevier B.V. All rights reserved.more varied shapes of
uramerican Paleozoic; as
ere observed by Mamay
ecent part of the fossil
1978; Gilbert, 1
records of copro
are either record
and dispersed in
occurrences with
compression?im
commences with
stems of the ?laio).
l rights reserved.on average from 944?1190 ?m to 1065?1120 ?m, andReceived 29 November 2010 D'Rozario et al., from the Upper Permian deposits of Yunnan Province, southwest China. The distinctive
Article history: We report well-preserved cSpatiotemporal extension of the Euramer
the Late Permian of Cathaysia: In situ cop
Yunnan Province, southwest China
Ashalata D'Rozario a,?, Conrad Labandeira b,c, Wen-Y
a Department of Botany, Narasinha Dutt College, 129, Bellilious Road, Howrah 711 101, In
b Department of Paleobiology, National Museum of Natural History, Smithsonian Institutio
c Department of Entomology and BEES Program, University of Maryland, College Park, MD
d State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chines
e 2 Xiamen Environmental Protection Research Institute, Xiamen 361006, PR China
a b s t r a c ta r t i c l e i n f o
j ourna l homepage: www.an Psaronius component community to
lites in a P. housuoensis stem from
uo d,e, Yi-Feng Yao d, Cheng-Sen Li d
ashington, DC 20013-7012, USA
42 USA
ademy of Sciences, Xiangshan, Beijing 100093, PR China
matology, Palaeoecology
ev ie r.com/ locate /pa laeo979; Thompson, 1994). Detritivore and herbivore
lites occurring in permineralized Psaronius contexts
ed sporadically in coal-ball ?oras within plant tissues
to the ambient peat; or alternatively, have sparser
in tissues of isolated trunks, rachises, and foliage in
pression deposits. Evidence for Psaronius associations
pith borings inside the carbonate-permineralized
yered cells morphotype? during the latest Middle
Pennsylvanian, from the lateMoscovianHerrin Coal of the Illinois Basin,
in the United States (Lesnikowska, 1989; Labandeira et al., 1997;
Labandeira and Phillips, 2002). Psaronius associations especially expand
during the Late Pennsylvanian, particularly involving several herbivore
associations on carbonate-permineralized Psaronius chasei Morgan
vegetation from the Calhoun Coal of the Illinois Basin, including
distinctive but primitive galls that indicate the existence of insect
holometaboly (Lesnikowska, 1990; Labandeira and Phillips, 1996b;
2002; Labandeira, 2011). The pith borings in the Psaronius ?layered cells
morphotype? and chasei stems, consisting of spheroidal to ellipsoidal
coprolites with distinctive contents and ground-tissue fragments, and
are nearly identical to coprolites in P. magni?cus (Herzer) Rothwell and
Blickle stems from the Redstone Coal of the northern Appalachian Basin
in Ohio (Rothwell and Scott, 1983). By contrast, the Permian reveals
fewer instances of detritivorous or herbivorous associations of Psaronius
organs. R??ler (2000) reported small-sized coprolites in tunnels
representing oribatid mites in silici?ed adventitious roots of Psaronius
sp. from the Lower Permian (Asselian) of Chemnitz, in the Erzgebirge
Basin of Germany; however, he did not ?nd larger, insect-like coprolites
in the cortical parenchyma, as in Pennsylvanian-age specimens from the
United States. By contrast, Permian compression?impression record
from north-central Texas had fewer instances of detritivorous and
herbivorous associations, and consumption of Psaronius-af?liated
Pecopteris foliage either was virtually absent in the case of the Lower
containing well-preserved plant debris within the permineralized
marattialean tree fern stem, Psaronius housuoensis (D'Rozario et al.,
2011), from the Upper Permian (Lopingian) of China, providing
additional?in our case latest Paleozoic?data on this unique assem-
blage of plant?animal associations.
2. Materials and methods
We collected material for the present investigation from Upper
Permian deposits of the Housuo Coal Mine, Fuyuan County, Yunnan
Province, southwest China. This deposit is assigned to the Xuanwei
Formation, of transitional Wuchiapingian to Changhsingian age (Hilton
et al., 2004). Preservation occurs as permineralized fossil trunks in the
coal mine. Other taxa in this ?ora include the calamitalean sphenopsid
Arthropitys yunnanensis (Wang et al., 2006), and some preserved
Psaronius stems (Hilton et al., 2004). Most of the Housuo Flora remains
undescribed.
Thepermineralized specimenof a 23 cm long Psaronius housuoensis
stem was cut into several, thin, transverse sections with a rock saw
(model SPOJ-300). The resulting slabs were ground and polished with
100 to 300 grit carborundum powder, and mounted onto glass
microscope slides using epoxy resin and triethanolamine. The slide
slabs were further polished with 600 to 1000 grit of carborundum
powder on a glass plate to achieve an optical thickness for observation
al. s
ste
cler
opr
e ce
=1
ing
ue.
sca
m t
aqu
; sc
S-2
lite,
Slide
06;
3; s
ate
lite.
; sca
chy
a a
128 A. D'Rozario et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 306 (2011) 127?133Permian (late Sakmarian) Coprolite Bone Bed Flora (Labandeira and
Allen, 2007), or occurs at (very) low levels in other, similarly aged Texan
?oras that have beenpreliminarily studied (Beck and Labandeira, 1998).
Notably, it is the seed plants, particularlymedullosan and gigantopterid
pteridosperms, that overwhelmingly display the highest herbivory
levels in these compression ?oras (Labandeira, 2006a).
Reports of coprolites from China are rare and there are no previous
instances of their occurrence within the stems of Chinese Psaronius.
Hilton et al. (2001) recorded plant damage and coprolites from the
Yangshuling Mine, from the Pingquan District of Hebei Province,
northern China, that were assigned to the Early Permian Taiyuan
Formation of northern China. However, the coprolites contained
mostly unrecognizable plant fragments dispersed among unaf?liated,
permineralized plant fragments (Seyfullah et al., 2009). The only
identi?able Taiyuan coprolites were those that occurred within the
Myeloxylon rachis of a medullosan pteridosperm. The present
contribution records for the ?rst time the occurrence of coprolites
Plate I.
1. Cross section of the examined stem of Psaronius housuoensis D'Rozario et
coprolites occurring among highly decomposed, structureless tissue. The
vague interstelar parenchyma, and is bounded outward by a thin zone of s
HS-27-10; scale bar=10 mm.
2. A part of the stem, enlarged from (1) at left, showing compactly disposed c
celled and thicker walled xylem (tracheids with white centers) toward th
celled phloem (with occluded, brown centers). Slide HS-27-02; scale bar
3. Portion of the stem enlarged from (2) at left, exhibiting coprolites contain
with opaque centers, stem parenchyma, and xylem-rich vascular tiss
bar=100 ?m.
4. Eight xylary tracheids linearly arranged within a coprolite, each showing
5. Enlargement of a tracheid similar to one at left in (4), showing scalarifor
6. Coprolite containing parenchyma and embedded gum-sac cells (with op
7. A kidney shaped sclerotium, occurring within a coprolite. Slide HS-27-12
8. A second kidney-shaped sclerotium, occurring within a coprolite. Slide H
9. A distinctive, triangular-shaped, spinose spore, occurring within a copro
10. An ovoidal fungal sclerotium, with spores, occurring within a coprolite.
11. Two spheroidal fungal sclerotia, with spores, in a coprolite. Slide HS-27-
12. A cylindrical fungal sclerotium, with spores, in a coprolite. Slide HS-27-1
13. Six fungal, spore-bearing sclerotia of various shapes, including a polylob
14. An ellipsoidal, spore-bearing fungal sclerotium at center, within a copro
15. An ovoidal fungal sclerotium, with spores, in a coprolite. Slide HS-27-16
16. Stem contents containing scattered, angular fragments of probable scleren
among empty space. Slide HS-27-09; bar=100 ?m.
17. Plant tissues within a coprolite containing Psaronius-degraded parenchymstructures also are present. Slide HS-27-12; scale bar=50 ?m.under transmitted and re?ected light .The slides were observed and
studied by a Leica DMREmicroscope, a Leica DM 2500microscope and
an Orient SMI stereo microscope, photographed with Nikon Coolpix
4500, LeicaDFC 420 and CannonEOS 20Ddigital cameras. Imageswere
adjusted in Adobe Photoshop (V. 7) and plates prepared in Corel
Draw (V. 12). All specimens and prepared slides are deposited in the
Palaeobotanical Laboratory, Institute of Botany, Chinese Academy of
Sciences, Beijing.
3. Observations
Transverse sections of the entire length of the petri?ed stem of
Psaronius housuoensis exhibits a well preserved, polycyclic dictyostele
embedded within poorer preserved parenchymatous ground tissue
(Plate I, 1). Tracheary elements of the xylem are undisturbed andmost
of the parenchymatous ground tissue is either degraded to amor-
phous masses (Plate I, 1?2), or is completely replaced by well-packed
howing separate meristeles of the polycyclic dictyostele and ground tissue replaced by
m consists of an inner region with looping sheets of tracheid-bearing vascular tissue,
enchyma; a distinctive root mantle occurs beyond the outer periphery of the stem. Slide
olites occurring among highly degraded, structureless parenchymatic tissue. Note larger
nter of the meristeles, surrounded on the periphery by thinner walled andmuch smaller
0 mm.
identi?able Psaronius plant tissues, principally tracheids as linear features, gum-sac cells
Note unconsumed vascular tissue strand at bottom margin. Slide HS-27-15; scale
lariform thickenings. Slide HS-27-01; scale bar=100 ?m.
hickenings. Slide HS-27-01; scale bar=50 ?m.
e contents). Slide HS-27-08; scale bar=100 ?m.
ale bar=50 ?m.
7-14; scale bar=50 ?m.
characterized by linear spines along its periphery. Slide HS-27-12; scale bar=50 ?m.
HS-27-03; scale bar=50 ?m.
scale bar=50 ?m.
cale bar=50 ?m.
form, in a coprolite. Slide HS-27-07; scale bar=50 ?m.
Slide HS-27-14; scale bar=50 ?m.
le bar=50 ?m.
ma, degraded parenchyma cells, and cross-section of tracheids in xylary vascular tissue,
nd conspicuous gum-sac cells containing opaque centers; occasional spheroidal fungal
129A. D'Rozario et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 306 (2011) 127?133
130 A. D'Rozario et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 306 (2011) 127?133fecal pellets that occur among the amorphousmaterial (Plate I, 2). The
coprolites are subcircular to ovoidal in shape, and rather uniform,
ranging in size from 944?1190 ?m to 1065?1120 ?m. and vary from
dark to light brown in external color (Plate I, 3). They are composed of
plant remains containing mostly fragments of indurated tissue
particles represented by tracheids (Plate I, 4?5), parenchyma and
contained gum sac cells (Plate I, 6, 17), spore-bearing fungal sclerotia
(Plate I, 7?8, 10?15, 17), triangular-shaped, spinose spores (Plate I, 9),
and other non-identi?able plant matter (Plate I, 16?17). The fragmen-
tary tracheids within the coprolites have scalariform thickenings (Plate
I, 4?5). The fungal sclerotia are all spore-bearing and occur in a variety of
shapes, including reniform (Plate I, 7?8), ovoidal (Plate I, 10, 15),
spheroidal (Plate I, 11), cylindrical (Plate I, 12), polylobate (Plate I, 13),
and ellipsoidal (Plate I, 14, 17), and other shapes (Plate I, 13). Lastly,
embeddedwithin the amorphous parenchymatousmatter surrounding
the coprolites and other stem tissue are occasional occurrences of
scattered, angular fragments of parenchyma, xylary tissue, and possible
sclerenchyma, as well as enigmatic ovule-like structures, surrounded
by empty space (Plate I, 2, 16). The stem is surrounded by a mantle of
adventitious roots (Plate I, 1).
4. Discussion
The single petri?ed stem shows anatomically well-preserved
tracheids and poorly preserved ground tissue, which has been replaced
mostly by fecal pellets and sediments. The coprolites, in turn, contain
tracheids and other vascular tissue, parenchyma, fungal remains
and non-identi?able plant matter that occupy an irregular tubular
volume that is approximately 3.5 cm in diameter (Plate I, 1). This
indicates that the food source of the coprolite-producing organism was
Psaronius stem parenchyma, and the identity of the culprit was a pith-
boringmyriapod or insect. The suspect myriapod or insect that invaded
the partly rotted stemof Psaronius housuoensis, eventually consumed its
way through partially decomposed parenchymatic tissue and empty
spaces formed by the ongoing decomposition process. In the process,
the culprit avoided the structurally more resistant vascular tissue,
peripheral sclerenchyma and root mantle, while simultaneously
depositing fecal pellets (e.g., Wallwork, 1976; Ausmus, 1977). The
comparatively intact and pristine vascular tissue, outer sclerenchyma
band and root mantle indicate that in the ambient decomposing
environment, the parenchymatous ground tissue decayed earlier than
more ligni?ed elements, also seen in stem tissues in older Euramerican
Psaronius plants (Rothwell and Scott, 1983; Labandeira, 2001). The
insect or possibly myriapod occupied the partly rotted stem and
deposited fecal pellets while advancing through the decaying paren-
chyma cells, causing further decomposition, such that only partial and
amorphous ground tissue remain.
Based on coprolite contents and tunneling preferences in the stem,
themyriapodor insect depositing the fecal pellets did not feedonmore
indurated tissues of the P. housuoensis plant. This is evident from the
near pristine microanatomical condition of the xylem from both the
stem and root of this plant, albeit some xylary tissuewas consumed, as
evidenced by tracheids in the coprolites. As there is no abundant
occurrence of extraneous plant debris among the coprolites, except
possibly a few scattered plant fragments and ovule-like structures, the
likelihood that coprolites were washed into the stem from the
surrounding environment is minimal. Moreover, the juxtaposition of
the coprolites indicates that they were extruded as a string of fecal
pellets from an endophytic insect, rather than being washed in as
particles from the ambient environment. These myriapods or insects
therefore must have fed on the constituent ground parenchyma of the
stem pith, as evidenced from coprolite contents of collapsed
parenchyma cells and especially distinctive gum-sac cells with opaque
centers of a resinous substance. This further indicates that the
coprolites were deposited and preserved in situ, within the stem.
This condition is similar to that reported byR??ler (2000) for Psaroniussp, by Rothwell and Scott (1983) for P. magni?cus, and by Labandeira
and Phillips (2002) for P. chasei, in which the ground tissue was
consumed, evident by the presence of fecal pellets that contain tissue
fragments and cell types representing Psaronius parenchyma. The
presence of fungal sclerotia in the coprolites indicates secondary
colonization by saprobes soon after fecal-pellet deposition.
4.1. Who was the myriapod or insect culprit?
The myriapod or insect involved in this association with P.
housuoensis evidently was a litter-dwelling, pith-boring arthropod
occurring within hardened tissues that exhibit early signs of decay.
This conclusion is based on the known microhabitat, pattern of
tunneling, absence of any evidence for herbivory on stem tissues, and
coprolite contents. The presence of fungi in the coprolites indicates
that colonization of the coprolites occurred soon after the stem
became necrotic and possibly after the death of the causative
arthropod. These fungal sclerotia within the coprolites may represent
multiple genera, based on shape and spore size, and evidently were
secondary colonizers of coprolites and plant tissues, a recurring
pattern seen in late Paleozoic coal balls such as the Calhoun Coal
(Agashe and Tilak, 1970; Baxter, 1975; Wu et al., 2007).
General evidence indicates that the principal herbivores of the
Pennsylvanian and Permian were arthropods, in particular smaller
sized mites and larger sized myriapods or insects (Hughes and Smart,
1967; Scott, 1977, 1980; Labandeira et al., 1997; Labandeira, 2001,
2006b). In addition to oribatid mites, which represent the small-borer
detritivore guild (Labandeira et al., 1997), there are a variety of
myriapods and insects that bore into various indurated and softer
plant tissues that typically fabricate order-of-magnitude larger tunnel
diameters, consistent with the dimensions of the P. housuoensis pith
boring. A possible candidate is a myriapod, such as a diplopod or
immature arthropleurid (Rolfe, 1969), which fed primarily on decay-
ing plant matter, especially rotting stems and foliage (Rolfe and
Ingham, 1967; Rolfe, 1969, 1983). Dawson (1860, 1878), for example,
reported the occurrence of the fossil diplopod Xylobius sigillariae in a
Sigillaria stem. Members of the extinct class Arthropleurida inhabiting
Carboniferous coal measures have been reported by Rolfe and Ingham
(1967) to be phytophagous and the gut contents of the myriapod
Arthropleura armata contained remains of carbonized tracheids with
scalariform thickenings and epidermal fragments of lycopod af?nity
(Rolfe, 1969). However, the last known arthropleurids are of earliest
Permian (Asselian) in age, and probably were long extinct by the end
of the Permian.
In addition to diplopods, Late Permian insect culprits responsible
for the boring would be those for which some knowledge of
endophytic penetration of dead plant tissues is available, such as
springtails (Collembola), cockroaches (Blattodea), and orthopterans
(Orthoptera) (Chopard, 1938; Chotoko, 1977; Lasebikan, 1977; Rolfe,
1983;Hopkin andRead, 1992:Hopkin, 1997;Nalepa et al., 2001).More
likely culprits are the larvae of phylogenetically basal lineages from
several holometabolous insect orders (Labandeira and Phillips, 2002;
Labandeira, 2011). Many larvae of holometabolous insects, particu-
larly beetles (Coleoptera), are consummate wood borers (Blackman,
1922; Fukuda, 1941; Hamilton, 1978; Crowson, 1981), but there are
larvae from other basal lineages, especially saw?ies (Hymenoptera),
scorpion?ies (Mecoptera), and lacewings and relatives (Neuroptera)
that also are plausible (Gallard, 1932; Burdick, 1961; Pilgrim, 1972;
Togashi, 1989; Byers, 1991). These, basal lineages of holometabolous
insects were present during the Late Permian, based on phylogenetic
and fossil evidence (Beutel, 2005; Ren et al., 2009; Vilhelmsen, 2009).
Curiously, these basal lineages are commonly associated with
xylophagy, wood-boring and/or bark-inhabiting habits, such as
archostematan beetles, known from the Upper Permian (Geertsema
and van der Heever, 1996; Beckemeyer and Engel, 2008), symphytan
hymenopterans whose earliest fossil occurrence is the Middle Triassic
131A. D'Rozario et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 306 (2011) 127?133(Riek, 1955), both taxa undoubtedly existed during the Late Paleozoic
based on diverse phylogenetic evidence (Vilhelmsen, 2009). The
nannochoristid and related Mecoptera have larval life-habits also
consistent with a detritivorous, moist environment, as indicated by
Beutel et al. (2009) who describe later instars of the larva of
Nannochorista philpotti as occurring ?? in damp (e.g., bryophyte)
vegetation or under bark of decomposing, partially submerged logs?
(p. 428).
The existence of detritivore pith borer during the Late Permian on
Psaronius housuoensis stem from China is an extension of a functional
feeding group whose earliest occurrence is on the ?layered-cells
morphotype? species from the Euramerican Middle Pennsylvanian
(Labandeira and Phillips, 2002). Occupants of this feeding niche
undoubtedly turned over taxonomically from the late Middle
Pennsylvanian through the Late Permian, as lineages of insect pith-
borers were extirpated and replaced by other lineages having the
same trophic roles. This processwas not only long-ranging during a 50
million-year interval, but also widespread biogeographically, shifting
from Euramerica to Cathaysia. Given what we know of insect
extinction and origination patterns for this interval (Labandeira,
2005), it is highly unlikely that there was any taxonomic carry over in
pith-boring arthropods from the late Middle Pennsylvanian (Herrin
Coal) of Euramerica to the Late Permian (Housou Coal) of the South
China Block. A simple test of this inference can be made by body-fossil
identi?cations of arthropod remains associated with this type of
coprolite in other Psaronius pith-borings.
4.2. The Psaronius component community in time and space
Currently, the most persistent, Paleozoic community of associa-
tions for a single source?plant taxon is in Euramerican Psaronius and
its detritivores and herbivores. Variable occurrences of these associ-
ations are known for at least ?ve deposits ranging in age from late
Middle Pennsylvanian (Herrin Coal) to the Late Permian (Housuo
Coal), spanning most of the Euramerican equatorial belt and now
the paratropical South China Block (Rothwell and Scott, 1983;
Lesnikowska 1990; Labandeira and Phillips, 1996a, 1996b, 2002;
Labandeira et al., 1997; R??ler 2000; this report). To date, the most
diverse nexus of associations at a single locality was documented for
Psaronius chasei Morgan from the Late Pennsylvanian Calhoun Coal,
which featuresmite, myriapod, and insect detritivory (Labandeira et al.,
1997; Labandeira, 2001), includingmite coprophagy of insect herbivore
coprolites (Labandeira, 2001, unpublished), as well as varied herbivory.
The insect herbivore associations involve consumption of various organ
form-genera, and include external foliage feeding, as surface abrasion, of
Pecopteris pinnules (Labandeira, 2001, unpublished); piercing-and-
sucking of xylary tissue of Stipitopteris rachises (Labandeira and Phillips,
1996a); galling of Stipitopteris rachis inner parenchyma (Lesnikowska,
1990; Labandeira and Phillips, 1996b, 2002); stem boring of Psaronius
trunk ground parenchyma (Labandeira, 2001; Labandeira and Phillips,
2002); palynivory of combined Scolecopteris sporangial tissue and their
Punctatisporites spores (Labandeira, 1998a, 2000, 2001); and root
feeding onaerenchymatous tissue (Labandeira, 2001), (a brief summary
of the P. chasei component community from the Calhoun Flora, is
presented in Labandeira (1998b, 2001), which lists several examples of
the varied types of herbivore-in?icted damage to a variety of plant
tissues). The pervasiveness of these Psaronius associations in time and
space constitute a component community, as de?ned by Root (1973),
speci?cally a source host-plant and all consuming herbivores and other
trophically dependent detritivores, predators and other nutritionally
derivative feeding guilds (also see Lawton, 1976).
The spatiotemporal recurrence of Psaronius associations resembles
thatof a tightly integratedmicroecosystem, such thatboth theherbivore
associations and the congeneric host-plants co-occur in multiple
(currently ?ve), Late Carboniferous to Late Permian deposits in
Euramerica, and now Cathaysia (Rothwell and Scott, 1983; Labandeiraand Phillips, 1996a, 2002; R??ler 2000, this report). The spatiotemporal
co-occurrence of the Psaronius host and its associated herbivores and
detritivores is evidence for an ecologically enduring association during
the Late Paleozoic. However, evidence for recurrence of associations is
insuf?cient (albeit necessary), by itself, for positing true co-evolution
(Thompson, 1994). True co-evolution in the fossil record requires, in
addition to spatiotemporal co-occurrence, a testable mechanism for
explaining a mutualism or other associational type (Thompson, 1994),
and, in addition, reciprocal genetic feedback in the case of modern taxa
(Janzen, 1980). This former condition?a plausible co-evolutionary
mechanism?is not demonstrable in the Psaronius case. Nevertheless,
as a recurring set of af?liated associations, now variably expressed in
?ve deposits, the Psaronius system of detritivores and herbivores is
the most pervasive plant?arthropod association in the Paleozoic fossil
record.
4.3. Summary
The following four points encapsulate the major ?ndings of our
discovery, including description of the specimen, and inferences
derived from this and related, late Paleozoic material.
1. A petri?ed specimen of the marattialean tree fern, Psaronius
housuoensis (D'Rozario et al., 2011) was found in the Late Permian
Housuo Coal from southwest China. Structural details and contents
of a longitudinal tunnel through the stem indicate that it was made
by a detritivorous, pith boring, terrestrial arthropod that inhabited
the litter zone.
2. Attribution of the P. housuoensis stem tunneler to a particular
diplopod or insect clade is impossible because of the absence of
body-fossil evidence. Through consideration of evidence such as
the details of the boring, coprolite structure, geochronological
window of occurrence, and arthropod phylogeny, suggests that
the fabricator most likely is a holometabolous larva, possibly a
beetle.
3. This occurrence expands the component community of Psaronius
detritivores, herbivores and other trophically dependent feeding
guilds, ?rst noted in the late Middle Pennsylvanian of Euramerica,
and now the Late Permian of the South China Block of Cathaysia.
4. The approximate 50 million-year duration of the Psaronius com-
ponent community, and its occupation of multiple feeding guilds of
detritivorous and herbivorous arthropods in equatorial habitats
on two paleocontinents, indicates that it is the most persistent
terrestrial plant?arthropod association in the Paleozoic fossil
record.
Acknowledgements
This research work was supported by the Chinese Academy of
Sciences (CAS)?TWAS, the academy of sciences for the developing
world Visiting Scholar Fellowship award (2006, 2009) to ADR at
the State Key Laboratory of Systematic and Evolutionary Botany,
Institute of Botany, Chinese Academy of Sciences, Beijing. Thanks
are due to Bin Sun and Finnegan Marsh for preparing and formatting
the images of the photographic plate. The constructive suggestions
and comments by three reviewers are gratefully acknowledged. This
is contribution 180 of the Evolution of Terrestrial Ecosystems con-
sortium at the National Museum of Natural History, in Washington,
DC.
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