What Does the Occurrence of Sporormiella (Preussia) Spores Mean in Australian Fossil Sequences?

JOURNAL OF QUATERNARY SCIENCE (2018) 33(4) 380–392 ISSN 0267-8179. DOI: 10.1002/jqs.3020

What does the occurrence of Sporormiella (Preussia) spores mean in Australian fossil sequences?

JOHN DODSON1,2 and JUDITH H. FIELD1* 1School of Biological, Earth and Environmental Sciences, University of New South Wales, NSW, Australia 2State Key Laboratory of Loess and Quaternary Geology, Institute of Earth Environments, Chinese Academy of Sciences, Xi’an, Shaanxi, China Received 26 October 2017; Revised 9 January 2018; Accepted 14 January 2018

ABSTRACT: Understanding the loss of the ﬁnal few species of Australian megafauna is beset by a paucity of data on human arrival, well-provenanced megafauna, human/megafauna population range and distribution (coexistence and interaction), and the range, scale and impact of environmental changes spanning the human–megafauna period. To overcome these shortcomings, the occurrence and decline of coprophilous fungal spores of Sporormiella in sediments have been used as a proxy for extinct megaherbivores. The Sporormiella evidence is presented as the key indicator of extinction timing and these reports are often from locations where there is no known archaeological record or megafauna remains. However, interpreting fungal spore occurrence is not straightforward, as demonstrated by studies investigating taphonomy, taxonomy and the types of animal dung where Sporormiella occurs. No detailed studies on these problems exist for Australia and no evidence supporting the use of Sporormiella as a valid proxy has been reported. Here we examine the occurrence of Sporormiella spores from Cuddie Springs in south-eastern Australia. Despite a well-preserved suite of megafauna fossils, Sporormiella occurrence is sporadic and frequencies are low. We conclude that using Sporormiella alone as an indicator for the presence of megafauna is premature for the Australian context. Copyright # 2018 John Wiley & Sons, Ltd.

KEYWORDS: Cuddie Springs; megafauna extinctions; megaherbivores; palaeoenvironment; Sporormiella.

Introduction sequence is further informed by a palaeoenvironmental record, providing insights into the changing climatic conditions through The global extinction of a suite of animals termed megafauna has the formation of the fossil record (Field et al., 2002). The Cuddie attracted the attention of a wide range of researchers who look to Springs site has attracted controversy from some, who claim the explore the various drivers in these events (e.g. Martin and Klein, megafauna–human record must have accumulated through 1984; Koch and Barnosky, 2006; Field et al., 2008; Nogues- fluvial activity (e.g. Gillespie and Brook, 2006; Grun€ et al., Bravo et al., 2010; Brook et al., 2013; Wroe et al., 2013; Stuart, 2010). In fact, the setting makes this extremely unlikely (Field et 2015). Recently, several papers have used the occurrence of al., 2008). The arguments for significant site disturbance are Sporormiella spores (now referred to as Preussia sp.: Arenal et al., based on aspects of the optically stimulated luminescence (OSL) 2007; Kruys and Wedin, 2009; Mapperson et al., 2014; Kruys, single grain results, and the electron spin resonance (ESR)/U- 2015) to indicate the presence of megaherbivores, including for series dating (Grun€ et al., 2010). These criticisms have been Sahul (Late Pleistocene Australia–New Guinea). The authors (e.g. vigorously defended in context (e.g. Field et al., 2008, 2013; Rule et al., 2012; van der Kaars et al., 2017) interpret a downturn Fillios et al., 2010; DeSantis et al., 2017), and we will again in Sporormiella spore frequencies as evidence for megafauna return to this issue in the site description below. decline and extinction. The demise of the megafauna in Sahul, There is fragmentary evidence of megafauna in archaeolog- whether climate, humans or some combination of factors as the ical sites from other localities: a single Diprotodon element prime driver, has become a long running and sometimes fragment and putative Genyornis eggshell fragments from the acrimonious debate. The thin evidence base with respect to south Australian site of Warratyi (Hamm et al., 2016); late secure dates on fossil megafauna, most particularly terminal survival of Sthenurines at Seton Rockshelter on Kangaroo dates; the paucity of in situ fossil records; consensus on first Island, (McDowell et al., 2015); and four extinct species from arrival of colonizing humans and subsequent dispersal in Sahul; Nombe Rockshelter in the New Guinea Highlands (see coupled with no clear understanding of, or consensus on the Sutton, et al., 2009). Elements of a Sthenurine kangaroo, in timing and severity of climate changes in the late Pleistocene, pre-human levels at Cloggs Cave were thought to be c. 30 ka continues to polarize the megafauna extinction debates. (Flood, 1973), but reanalysis indicates 40 790–36 880 cal a bp (Flood, 2013). The fossil record is scant and reconstructing Megafauna and humans in Sahul (Pleistocene any potential relationship between megafauna and humans is Australia–New Guinea) challenging (Field and Wroe, 2012). On the modern Australian continent only one site has a clear spatial and temporal sequence of megafauna and humans the Human overkill in Sahul? late Pleistocene archaeological site of Cuddie Springs (Fig. 1) (Dodson et al., 1993; Field and Dodson, 1999; Field et al., The human overkill model for megafaunal extinctions assert that 2008, 2013; Grun€ et al., 2010; DeSantis et al., 2017). The most, if not all, megafauna persisted on the Sahul continent until the arrival of colonizing humans, when human hunting and/or Correspondence: Judith H. Field, as above. habitat modification drove the extinction process (Johnson, E-mail: [email protected] 2006). There is no empirical evidence to conclusively support

Nombe Rockshelter

Madjedbebe

Lynch’s Crater Carpenter’s Gap Murubun

Coral Bay

Warratyi Cuddie Springs Upper Swan Willandra Lakes Devil’s Lair Seton Rockshelter Core MD03 2614G Cloggs Cave

SAHUL -130 m MODERN COASTLINE

0 500 1,000 km

Figure 1. Map of Sahul showing locations mentioned in text. Sahul shoreline is shown at 130 m from present-day sea levels. human overkill, or in fact one of climate change (Field and sequences are rare or absent. Fossil Sporormiella spores as Wroe, 2012). It appears that only 4–8 of more than 50 species indicators of dung from megaherbivores have been reported of megafauna may have overlapped with people and a shortage in the literature since 1977 (Davis et al., 1977). Davis (1987) of empirical evidence inhibits headway on the extinction and Davis and Shafer (2006) noted that spores were common question (Wroe et al., 2013). Although new data are starting to in sediments after grazing livestock were introduced, but emerge (e.g. Price et al., 2017), we know little of population were rare in the mid-Holocene. It was noted that Sporor- biology and habitat ranges of now extinct faunal species with miella abundance declined in the late Pleistocene, presum- which to understand the role of megafauna in either habitat ably when most large herbivores had disappeared. maintenance or change. Rule et al. (2012) and others have A link between Sporormiella and mammoth dung was argued that there was significant habitat change after the demise demonstrated by Davis and colleagues, reinforcing their use of of the megafauna, but until the timing and rates of the demise of Sporormiella as a proxy for megaherbivores in North America. megafauna is established across environmental zones, then it is At Wildcat Lake in Washington State, Davis et al. (1977) found difficult to make this call (Wroe et al., 2013). While there have abundant Sporormiella spores in two sediment levels where been significant changes in vegetation structure through Marine introduced grazing animals were present, but were rare before Isotope Stage 3 (MIS-3), most notable shifts in vegetation this time. The presence of Sporormiella was not consistent and communities are complex and often result from a combination they argued that the degree of slope wash may have been an of factors. Attributing primary causes to extinctions events is important factor in their representation. Gill et al. (2009) noted therefore problematic (Wroe and Field, 2006), and explains in the close correlation between megaherbivores, fire and vegeta- part why researchers have turned to proxy evidence from the tion but could not attribute their decline to one specific factor. fossil record as indicators of megafaunal decline. In Madagascar, Burney et al. (2003) reported the decline of Sporormiella spp. in well age-constrained sediments at about 1720 14C a bp, just preceding a major human transformation Dung fungus and megaherbivores of the landscape by fire. Notably, spore percentages were Coprophilous fungi have been identified as a potentially always low in some montane sites but values generally rose useful indicator of megaherbivore presence where fossil fauna after the introduction of livestock.

Since the first link between Sporormiella and megaherbi- 1986a, 1986b). Wood and Wilmshurst (2012) investigated vores was demonstrated, there has been a wealth of literature the differences in spore frequencies and correlation to on Sporormiella as a proxy for megafauna, especially from extinction events between wetland and relatively dry soil North America. There is no clear consensus on the interpreta- sequences in New Zealand. A better correlation with extinction of these data. For example, Robinson et al. (2005) tions was observed in the latter, reinforcing the need for investigated Sporormiella and fire histories as related to careful consideration of hydrological conditions in lakes. human activities and megafaunal decline, and concluded the However, for Australian contexts, in locations where annual extinctions were human-mediated. Conversely, Emery-We- precipitation is low, e.g. the arid/semi-arid zones, the survival therell et al. (2017) find the data across North America of pollen or spores can be severely constrained and often inconclusive for identifying a single causal agent in the only found in ephemeral lake deposits. Nonetheless the larger demise of the megafauna. issue of spore survival and lake hydrology remains and needs The source of Sporormiella spores in pollen sequences and to be considered for each location. their correlation to extinct megaherbivores, or extant faunal Johnson et al. (2015) analysed Sporormiella and other species, in Australia has not been well studied. Rule et al. fungal spores in Lynch’s Crater core sediments from tropical (2012) suggest, but do not demonstrate, that spores are north-east Queensland. Spores were present in all samples, known from the dung of existing large herbivores such as decreasing at about 40 000 a bp then persisting in reduced kangaroos and emus, and introduced animals such as cattle. numbers after this time. The study focused on taphonomic The same correlation has not been demonstrated for Sahul issues as revealed in two cores from the site. Confirming the megafauna, but there are no reports of preserved megafauna Raper and Bush (2009) study, they demonstrated spatial dung to our knowledge. Wood et al. (2011) found coprophi- variability of Sporormiella within the site, and that spatial lous fungi, including Sporormiella, are widely distributed in variability in representation is an important consideration. endemic New Zealand and Pacific island herbivores, namely The authors concluded that the major decline in spores birds which notably includes numerous species of now represented local megafauna extinction. Johnson et al. (2015) extinct Moa (Order Dinornithiformes). The same patterns explain subsequent peaks in Sporormiella as reflecting the could potentially be found in modern extant large Australian presence of extant species such as large kangaroos. birds such as the Emu (Dromaius novaehollandiae) and the Cassowary (Casuarius spp.). Sporormiella frequencies, faunal extinctions, humans and climate change in Sahul Fungal spore taphonomy Rainforest vegetation dominated the Lynch’s Crater surrounds Feranec et al. (2011) and Baker et al. (2013) have noted that at the time of the Sporormiella decline yet there are no the interpretation of Sporormiella abundance lacks critical known records of megafauna near the site, or indeed from taxonomic and taphonomic investigations. In various con- any Quaternary age rainforest in Australia. We can find no texts, spores are associated with rabbit scats, ground squirrel assessment of what the rainforest megafauna actually were, if and porcupines, as well as large mammals, yet we still have in fact any were present in these environments. We do know some way to go before we have a full understanding of what numerous extant species including tree kangaroos, casso- the spore abundance actually means (e.g. van Asperen, 2017; wary, some wallabies and other small marsupial fauna (e.g. Raczka et al., 2016). In tests for fungal spore diversity on Hypsiprymnodon) are found in modern-day rainforest con- modern dung samples, van Asperen (2017) found Sporor- texts. Furthermore, there are no archaeological sites older miella was present on only one elephant dung sample, was than ca. 30k 14C a bp known from this region. Murubun rare on two feral animal samples and genuinely absent from Rockshelter where excavations documented a very low other samples. Significantly, van Asperen also concluded that artefact discard rate and probably only periodic site visitation it was unlikely that spores of coprophilous fungi from around 30k 14C a bp, was abandoned during the Last Glacial sediments could be used as a proxy to identify specific Maximum (LGM) (Cosgrove et al., 2007). The decline in megafaunal herbivore species (van Asperen, 2017). For any Sporormiella frequencies also tracked the decline in aquatic meaningful interpretations of Sporormiella abundance in the taxa at Lynch’s Crater, a consideration not fully explored by fossil record to be developed, it is essential to establish a Rule et al. (2012). With so many questions about the relationship between the occurrence of dung and the pres- interpretation of the Lynch’s Crater sequence, it is difficult if ence of Sporormiella (e.g. Basumatary and McDonald, 2017), not impossible to reconcile megafaunal extinctions with the as well as the association between suspected source animals fossil sequence at this site. and spores of Sporormiella. In explaining the Lynch’s Crater Sporormiella decline, Rule In their study of 15 Florida lakes, Raper and Bush (2009) et al. invoke a negative argument that no evidence for showed that abundance is very sensitive to distance from climate change during this period can be detected, and dung source, and concentrations declined precipitously with therefore humans drove the extinctions by overhunting. There distance. Similar correlations have been reported by Raczka is no evidence anywhere on the Australian continent that et al. (2016) and Parker and Williams (2012). Abundance in people hunted the megafauna. Furthermore, for this North the centre of sites (lakes) may represent precipitation and Queensland record, it is only after the expansion and re- stream inflow rather than numbers of animals, especially establishment of rainforests across the Atherton Tablelands when sequences are not directly associated with fossil that people began entering these environments. It is likely skeletal remains. Importantly, consideration of dung fungal that the development of technologies allowing the exploita- spore dynamics in the context of entire herbivore communi- tion of toxic starchy tree nuts facilitated this process (Cos- ties is required, as is routinely done for pollen and associated grove et al., 2007). Our current knowledge of rainforest use transport mechanisms. Water availability and humidity will by people and the broader settlement and subsistence also have a significant impact on spore production, although patterns challenges the unproven assumptions that underlie experimental studies indicate that some Sporormiella spp. are the Rule et al. (2012) and Johnson et al. (2015) conclusions. more tolerant of both reduced moisture and humidity than In a second study correlating dung fungus spore frequen- observed for other genera (Kuthubutheen and Webster, cies and megafaunal decline, van der Kaars et al. (2017)

Copyright # 2018 John Wiley & Sons, Ltd. J. Quaternary Sci., Vol. 33(4) 380–392 (2018) SPORORMIELLA SPORES IN AUSTRALIAN FOSSIL SEQUENCES 383 counted Sporormiella spores from marine core sediments occurrence of Sporormiella from source is distance-sensitive. taken about 100 km off the southern Western Australian In Australia, no fossil dung of megafauna is currently known modern coastline in over 1000 m of water. They noted a with which to test the spore–dung relationship, nor, to our decline in spore numbers between 45 and 43.1k 14C a bp, knowledge, has an analysis been carried out in sites where and concluded these patterns indicated the demise of megafaunal remains may co-occur. megafauna on the adjacent continent, invoking human Here we present a new pollen-spore record from Cuddie hunting of megafauna as the cause. van der Kaars et al. cite Springs which contains a stratified record of well-preserved records from Devil’s Lair (about 750 km west of the core site, megafauna bones, and in the upper levels this co-occurs with which has an archaeological record from ca. 50k 14C a bp, an archaeological record (Field and Dodson, 1999; Field and not associated with any megafauna), the Upper Swan et al., 2013). The already published in situ pollen diagram River (open) site (humans at 38 ka but again no megafauna), did not include counts of Sporormiella or other spores of Central Australia (where humans are not demonstrated to be coprophilous fungi (Field et al., 2002). The aim here is to present until 36–35k 14C a bp), and some burnt (and now describe the environmental setting from a new pollen and unverified) extinct Genyornis eggshell finds near Coral Bay spore record and to examine the abundance of Sporormiella on the Western Australian coast (Miller et al., 2016), about spores in sediments enclosing the bones of extinct mega- 1000 km NNW of the van der Kaars study site. There is a fauna. The Cuddie Springs sequence provides an opportunity dearth of dated megafauna from SW Australia, and the to compare environments and Sporormiella abundance in the archaeological record is scant at this time. presence of humans, and in times long pre-dating a human In the offshore core sequence, fungal spore numbers presence in Sahul from sediments deposited around 400 ka continued in small amounts after 40k 14Cabp,presum- (Grun€ et al., 2010; Field et al., 2013; DeSantis et al., 2017). ably representing the continuing occurrence of extant large herbivores. The claim that humans must have been The site the causal agent for the extinctions is at odds with the lack of corroborating evidence. For example, the burnt Cuddie Springs is a claypan in a larger lacustrine setting on Genyornis shells have no associated archaeology and the the north-west plains of New South Wales (Fig. 1). The claim as it stands is unsupported. Furthermore, the stratigraphy (Fig. 2) has been described in detail elsewhere identification of these eggshells as Genyornis has been (Meakin, 1991; Field and Dodson, 1999; Field et al., 2001, comprehensively refuted, and they are now attributed to 2002, 2008, 2013; Field, 2006; Field and Wroe, 2012). an extinct megapode, probably Progura sp., only 5–8 kg in Cuddie Springs is in a landscape of low relief and has not size (Grellet-Tinner et al., 2016, 2017). been part of any river system over the last ca. 900 ka (see van der Kaars et al. (2017) also claim there is no evidence Field et al., 2008; Grun€ et al., 2010). The modern-day site of a major climate shift at ca. 45 ka in Australia. These presents as an ephemeral lake approximately 3 km in diame- assertions are at odds with the recent work by Cohen et al. ter but may have formed initially as a terminal low back (2015), whom they cite but did not comment upon, docu- swamp between the Marra Creek floodplain and the slightly menting a major drying episode in Australia’s largest lake higher areas of red soils to the east. Drilling by the Geological basin (Lake Eyre) at about 48 2 ka. The drying episode Survey of New South Wales (Meakin, 1991) established that coincides with the earliest site reported for the Flinders from 38 m depth to approximately 12.6 m below the surface Ranges (Hamm et al., 2016) in which one (unmodified) the sediments comprise lacustrine silts and clays deposited in fragment of Diprotodon bone and putative Genyornis egg- a low-energy depositional environment. From 12.6 to approx- shell were found in sediments dated to 46–49k cal a bp. imately 3 m below the surface, a higher energy regime Human population densities across the Sahul continent at this persisted than in previous periods as suggested by the ‘angled time would have been very low (Williams, 2013), begging cross beds and fine sandy laminae’ of fine- to medium- the question of how so few people could have effected such grained, well-sorted sands. That section was probably related widespread faunal loss. The use of fire by people as a driving to high flood activity across the floodplain in the area and we agent in habitat reconfiguration is at odds with the low consider the lens pre-dates the materials in the present human densities across the landscape. Fire frequencies may analysis. not have changed much since the Pliocene (Atahan et al., The surface 1–3 m are lacustrine clays and these have been 2004; Dodson et al., 2005), and modern studies of fire in the interpreted as intermittent flood deposits (Meakin, 1991). Western Desert indicate that most damage is initiated by Excavations carried out by authors of the current paper, in wildfires (from lightning strikes). Interestingly, low-intensity proximity to the core where these sediments were taken, is at human-initiated fires increase biodiversity in habitat and the centre of a treeless pan at the lowest point in the lake fauna and both co-vary with climate: rainfall and wind floor. We established that the upper ca. 3 m of deposit (Bliege Bird et al., 2008). comprises lacustrine clays and silts, which are fine grained, There arise several key questions about the meaning of with no cross bedding evident. These lacustrine facies contain Sporormiella fossil spore occurrence in Australian sequences. a well-preserved pollen and spore record (Field et al., 2002). First and foremost is the need to demonstrate a clear There are also well-preserved bones of extant and extinct correlation with herbivorous megafauna. Since Sporormiella megafauna throughout the deposit, and in some layers these is probably widely associated with all herbivore dung, its are highly concentrated (Field and Dodson, 1999; Fillios occurrence will be complex in relation to megafauna. Until et al., 2010). In the upper ca. 1.7 m the fossil bones co-occur that correlation is demonstrated, it is overly ambitious to with an archaeological record. At about 1 m depth from the apply evidence from different biota and ecosystems in surface there is a hard compacted layer of stone and some Madagascar and North America to the Sahul context. Further- bone, which appears to represent a hiatus in deposition more, we would question how many large animals producing during a period of extended drying during the LGM. There how much dung are required to effect high frequencies of are no artefacts below ca. 1.7 m in the sequence. A fragipan, Sporormiella spores, in any sequence, let alone 100 km a dense, compacted horizon comprising a well-sorted bone offshore from the Australian mainland. Such questions be- and non-artefactual stone at ca. 1.7 m (P. Hesse, pers. come even more important when considering that the comm.) overlies a band of cemented ferruginized sands. The

Figure 2. The Cuddie Springs stratigraphic section (from Square F10), showing the various stratigraphic units and sediment facies. (Illustration: J. Field, M. Fillios, J. Wells.) in situ record of humans and megafauna occurs in Strati- probably key in preserving the record in the lower SU9 graphic Unit 6 between 1.7 and 1 m depth from the surface. section. The pollen and spore record shows the environment The approximately 200-m-diameter claypan, at the lowest of the lower bone horizon (SU9) was a light woodland, point on the lake floor, is the sink for local run-off in heavy dominated by a chenopod shrubland and herbfield. The rain events and generally fills to around 30 cm depth (Fig. 3). aquatic taxa are consistent with relatively shallow and still The lake can fill to nearly 1 m depth when the entire freshwater conditions. The fauna documented in SU9 include ephemeral lake fills (approximately 3 km in diameter) (Field Pallimnarchus sp., Procoptodon sp., Diprotodon sp. Zygoma- and Dodson, 1999). turus sp., Macropus titan, sp., Macropus sp., Sthenurus sp., Previous work established a sequence of megafauna, Protemnodon sp. and Phascolonus sp. The skeletal elements archaeology and palaeoenvironmental data (Dodson et al., from this horizon are well preserved with little or no 1993; Field and Dodson, 1999; Field et al., 2001, 2002, weathering, and some elements were articulated (Fig. 4a). 2008, 2013; Field, 2006; Fillios et al., 2010; DeSantis et al., Many of the skeletal elements show puncture marks and 2017). The top 2.2 m in the centre of the basin contains two crushing from crocodile teeth, with over 200 teeth (many horizons where bones are concentrated. The lower horizon from juvenile crocodiles), recovered from a trench 1 m 1.5 (Stratigraphic Unit 9, SU9) is devoid of artefacts and ESR/U- m 0.2 m (J. Garvey and J. Field, unpublished results; series analyses returned ages ranging between 379 and 580 Fig. 4b). The faunal remains are consistent with the site being ka, which Grun€ et al. (2010) presented as a weighted average a waterhole, the death assemblage mediated by crocodiles. mean of 400 ka. SU9 is overlain by a dense pale grey The bone layer in Stratigraphic Unit 6 (SU6; ca. 1.7–1.05 m compacted clay, in places highly laminated, which is depth) co-occurs with an archaeological record and includes interpreted as representing a period of aridity, and possibly bones from both extinct and extant faunal species. The lower some deflation (SU8). The formation of this grey clay was section of this unit has a faunal suite dominated by skeletal

Copyright # 2018 John Wiley & Sons, Ltd. J. Quaternary Sci., Vol. 33(4) 380–392 (2018) SPORORMIELLA SPORES IN AUSTRALIAN FOSSIL SEQUENCES 385

Figure 3. View of the excavations being undertaken on the Cuddie Springs claypan in 2007. (Photo J. Field.) elements of Genyornis netwoni, with many found as sepa- numerous isolated teeth. This layer probably arises from the rated articulations (Fig. 5). The vegetation profile in the lower reopening of a well in the 1950s during a dry spell, as part of SU6 consists of a saltbush shrubland around a shallow described by local farmers. It was not further considered. freshwater, low-energy system. The SU6 horizon accumulated between approximately ca. Stratigraphic Unit 6 covers the period where fossil mega- 30 and 40 ka based on radiocarbon and OSL dates, and fauna and an archaeological record overlap but is in fact two within this unit, the SU6A and SU6B ages overlap. ESR/U- stratigraphic units SU6A and SU6B. Capping SU6 is a series dating on bone places the age a little earlier than the deflation pavement at around 1.05–1 m depth (SU5), consist- other methods (Tables 2 and 3). We note, however, that these ing primarily of flaked and some ground stone artefacts results are consistent with this method producing ages ca. 10 interspersed with bone, teeth and charcoal. The stones that 000 years older than other dating methods applied to other comprise most of the upper surface of this pavement are very sequences (see discussion in Cosgrove et al., 2010; Field weathered, the underside is not and the pavement is et al., 2013). The different results obtained using the various bracketed by dates of ca. 22 and 33 ka (Table 1). The upper dating methods at Cuddie Springs has led to claims of mixing metre of deposit is primarily undifferentiated clays with of material/sediments at the site. We can rule out mixing evidence of bioturbation, but at approximately 50 cm from between the lower and upper bone beds by taphonomic and the surface there is a band of coarse sand containing geomorphological studies (Trueman et al., 2005; see also

Figure 4. (a) Stratigraphic Unit 9 during excavation in 2002. (Photo: J. Field.) (b) Close-up of articulated elements in SU9 (arrow). (Photo: J. Field.)

Figure 5. Separated articulations of Genyornis newtoni in ﬁne- grained sediments in Strati- graphic Unit 6B at Cuddie Springs. Tibiotarsus (TBT) on left, tarsometatarsus (TMT) on base at right and ﬁbula (F) lying across the top of the bones. (Photo: J. Field.)

Field et al., 2013). The geomorphic setting of the site in a agreement with ages reported from Cuddie Springs (West- landscape of low relief, a well-preserved pollen record away et al., 2017). Nonetheless, while humans have been indicating a shallow depositional environment, an electro- present in and around the Willandra Lakes since ca. 50 ka, magnetic survey demonstrating no river channels within 10 m no human–megafaunal association or interaction has been of the surface, and particle size analysis showing lacustrine identiﬁed there. At Menindee Lakes, to the north of the clays and silts all point to a low-energy environment (see Willandra Lake system, the remains of the largest kangaroo, Field et al., 2008; DeSantis et al., 2017). We also note that a Procoptodon sp., have been identiﬁed and date to 66–51 ka, recent series of ages on a Zygomaturus trilobus specimen of pre-dating the underlying archaeology by many millennia between 32 and 37 ka from Willandra Lakes is in broad (Cupper and Duncan, 2006).

Table 1. Radiocarbon and optically stimulated luminescence ages for Cuddie Springs.

Stratigraphic Depth Lab. no. Age (bp) Cal age bp Calendric age Material Method unit (cm) (CalPal_2007_HULU) (CalPal_2007_HULU)

1 Surface Beta 81385 1470 70 1395 72 1323–1467 Charcoal AMS 3 76 Beta 81376 14 820 70 18 161 271 17 889–18 432 Charcoal AMS 4 95 Beta 81375 5590 660 6381 55 6326–6436 Charcoal AMS 4 95 None 16 700 1200 Sediment OSL 4 95 Beta 44374 19 270 320 23 084 420 22 663–23 504 Charcoal 14C 5 97 None 27 000 2000 Sediment OSL 5 97 Beta 81377 28 770 300 33 250 454 32 796–33 704 Charcoal AMS 6A 107 Beta 81378 32 900 510 37 386 842 36 544–38 228 Charcoal AMS 6A 107 Beta 46170 28 310 200 32 718 342 32 375–33 060 Charcoal 14C 6A 110 None 30 000 2000 Sediment OSL 6A 110 ANUA13012 28 590 480 33 059 583 32 476–33 642 Charcoal ABOX-SC 6A 110 ANUA10011 28 740 340 33 207 489 32 718–33 696 Charcoal ABOX-SC 6A 114 Beta 44375 30 280 450 34 530 397 34 132–34 927 Charcoal 14C 6A 114 Beta 81379 33 660 530 38 884 1491 37 392–40 375 Charcoal AMS 6A 120 ANUA13019 32 000 120 36 394 964 35 429–37 358 Charcoal ABOX-SC 6B 131 Beta 81380 33 300 530 38 100 1201 36 898–39 301 Charcoal AMS 6B 138 Beta 81381 30 990 360 35 077 415 34 662–35 492 Charcoal AMS 6B 140 ANUA10012 28 780 350 33 247 488 32 759–33 735 Charcoal ABOX-SC 6B 140 ANUA12309 31 340 1000 35 907 1224 34 683–37 131 Charcoal ABOX-SC 6B 151 ANUod118a 35 400 2800 Sediment OSL 6B 154 Beta 81382 32 580 510 37 090 864 36 225–37 954 Charcoal AMS 6B 155 None 36 000 3000 Sediment OSL 6B 155 Beta 46171 29 570 280 33 877 340 33 537–34 217 Charcoal 14C 6B 156 Beta 81383 32 420 460 36 943 874 36 069–37 817 Charcoal AMS 6B 161 Beta 81384 29 170 360 33 584 104 33 174–33 994 Charcoal AMS

Acid Base Oxidation-Stepped Combustion (ABOX-SC) (Bird et al., 1999).

Copyright # 2018 John Wiley & Sons, Ltd. J. Quaternary Sci., Vol. 33(4) 380–392 (2018) SPORORMIELLA SPORES IN AUSTRALIAN FOSSIL SEQUENCES 387

Table 2. ESR/U-series ages for Cuddie Springs teeth samples from Stratigraphic Unit 6 (Grun€ et al., 2010).

SU Sample no. Specimen U-ESR age (ka) Early U uptake (ka) U-series (ka)

6A 2040/E10 5A 60 Isolated cf. Macropus rufus molar† 40 6; 41 732 3 <4.9 (LA) 6A 2037/H10 3A 59 M. cf. osphranter molar from part mandible 45 545 5 45.3 1.9 (LA) 6A 2031/E11 2A 15 Sthenurus sp. isolated incisor 45.3 1.9 (LA) 6A 2039/H10 2FB 16 Isolated M. rufus molar fragment 50 6; 48 6 † 6A 2035/E10 4D 159 Isolated Sthenurus sp. lower incisor 75 12/8; 69 11/8; 68 7; 63 7 13.5 3.8 (LA) 6A 1436/F10 Spit 20 Isolated cf. Pallimnarchus tooth >451; >466 6A 2032/E10 3C 21 Isolated Macropus sp. tooth 672 79; 622 73 6A 2036/H10 2A 3 Isolated Diprotodon sp. molar fragment 650 78; 668 77 6B 2034/G10 27B 1 Macropus titan mandible 30.7 2.6 (LA) 6B 2038/E10 SPIT 15 Molar from Protemnodon mandible 35.7 4.5 (LA) 6B 2029/G11 AL1 E Molar from Diprotodon optatum mandible 51 6; 51 6; 50 6

† Identiﬁed as intrusive (probably from SU7) during excavation in 1994 (see Field and Dodson, 1999). Recovered during wet sieving of excavated sediments, not an in situ ﬁnd.

There is also clear evidence of division between two decided to focus on Sporormiella for two reasons: (i) spores stratigraphic units within the SU6 unit. The bones of of Sporormiella have been observed to have better survival megafauna identified in SU6B include Genyornis newtoni, rates and as such are more easily detectable in sediment Diprotodon sp., Protemnodon sp., Macropus titan, Sthenurus preparations (see Kuthubutheen and Webster, 1986a, sp. Phascolonus sp. and Varanus priscus (Fillios et al., 2010). 1986b) and (ii) the palaeoecological literature has been While megafauna elements are mostly concentrated in SU6B, focused on this species rather than all fungal types and it flaked stone artefacts are found throughout SU6A and SU6B, was felt our observations would be more easily translated beneath, beside and next to extinct and extant faunal to other, similar studies. elements (Fig. 6). The flaked stone raw materials are Identification of Sporormiella spores, originally from four- dominated by silcrete, which is locally available, but also celled ascospores, follows Burney et al. (2003) and Bell includes phyllite, feldspar porphyry and quartzite. Notably, in (2005): spores with a width of 10–12 mm and a length of SU6A grinding stones appear for the first time, there is an about 20 mm, and with a characteristic sigmoid aperture. increase in the representation of extant fauna, as well as Sometimes these are linear tetrads (Burney et al., 2003; Bell, concentrations of flaked stone artefacts and macro-charcoal 2005), but none was observed in this study. The pollen slides (Field and Dodson, 1999). had other fungal spores including those much smaller than The lower (SU9) and upper (SU6A, SU6B) layers have Sporormiella, multi-cell units, various shapes and sizes and in several megafauna taxa in common although the species some cases as sections of 3–5 units of hyphae. It is possible diversity appears to have contracted significantly by the that some of these may have been spores of other coprophi- time SU6A/B formed (Fillios et al., 2010; see also DeSantis lous fungi but they were not identified here. et al., 2017). The data were entered into a spreadsheet and a pollen and spore diagram was prepared using Tilia and Tiliagraph software (Grimm, 1991). Sporormiella show far more variabil- Laboratory analysis and palynology ity when expressed as concentrations or influx values (Feranec Pollen preparations for this study were made on subsamples et al., 2011). Here the chronological sequence was not well with a mass of about 0.5 g. They were soaked overnight in enough defined between samples to estimate influx rates, most deionized water, then again overnight in 40% HF. The especially in the lower section (SU9). Values were expressed samples underwent routine preparation through 5% NaOH, as percentages of the pollen sum as widely used elsewhere acetolysis and washing in deionized water before mounting (e.g. Gill et al., 2013) and for consistency in interpretation in glycerol (Moore et al., 1991). Sieving was avoided as with other sites. We also recognize that percentage values are recommended by van Asperen et al. (2016). Counts were subject to change with pollen productivity change. Feranec done under magnification of 400 until at least 200 pollen et al. (2011) note that values above 2% suggest the occurrence of terrestrial taxa had been identified. Aquatic taxa, fern of large herbivores at a site, while Gill et al. (2013) suggested spores, Azolla spores and Botryococcus colonies were also the value of 2.8% of total pollen and spores. counted (outside the 200). Fungal spores were generally abundant and were counted in two categories: Sporormiella and all other fungal spores. While there are other species of Results dung fungi whose spores may be present in these sediments The pollen and spore diagram divides neatly into two main (see van Geel and Aptroot, 2006; Rule et al., 2012), it was sections using a total sums of squares analysis (Fig. 7). Pollen

Table 3. Cuddie Springs ages on tooth enamel by the ESR/U-series methods for Stratigraphic Unit 9 (Grun€ et al., 2010).

Sample no. Specimen Early U uptake (ka)

2059/F11 6D 17 ?Macropodidae enamel fragment 348 57, 347 55 2055/F11 6D 16 Macropus sp. molar fragment 429 53, 458 56 2058/F11 6D 1 Vombatidae 447 55 435 55 2028/F11 6D 16 Macropus sp. Isolated molar fragment 541 68, 445 72 2060/F11 8D 12 Isolated Diprotodon sp. part molar 569 80, 510 72

Recovered during wet sieving of excavated sediments, not an in situ ﬁnd.

Figure 6. Flaked stone artefacts (white arrowheads) and elements of extinct megafauna co-occur in SU6 at Cuddie Springs. (Photo J. Field.) preservation was very good, and weathered grains were rare. section probably reflects freshwater conditions in a slightly The lower section (SU9, 175–220 cm depth) has abundant wooded semi-arid landscape. The faunal assemblage in Casuarina and small quantities of Eucalyptus, Melaleuca, Acacia SU9 was relatively more diverse than the upper section and Dodonaea, and a dominant herb component of Poaceae, (SU6B/6A). However, the numbers of Sporormiella spores Asteraceae and Chenopodiaceae. The latter is likely to include were still comparatively low. The environment in the upper shrubby taxa such as Atriplex and Maireana,aswellas section suggests a more arid landscape around a freshwater herbaceous taxa. This assemblage equates to a woodland with a system, which is consistent with its formation in the lead shrubby and herbaceous understorey. The aquatic taxa all up to the LGM. indicate freshwater conditions and the high values for Azolla, Myriophyllum and Cyperaceae, and low values for Typha and Discussion Villarsia species all indicate a shallow and still freshwater system, which is consistent with the fine clay lacustrine The Cuddie Springs deposit contains a well-preserved pollen sediment. Total fungal spore content was relatively consistent at and spore record indicating an environment of shallow, about 10% of the pollen sum. Sporormiella spores were present relatively still, freshwater conditions. The microfossil record in very low values and were not seen in several samples. and the sediment facies of fine clay with little silt (Field and The upper section (SU6) contains a pollen record which Dodson, 1999) indicates a lacustrine and non-fluvial setting, is very well preserved and few grains show evidence of an interpretation confirmed by electromagnetic survey (see weathering or re-deposition. There are very low numbers of Field et al., 2008). Discrepancies in dating studies, interpreted tree taxa, and these include some Casuarina, Eucalyptus, by some researchers as indicating site disturbance, have no Acacia, Melaleuca and Gyrostemonaceae. Poaceae, Aster- support in the systematically compiled site data investigating aceae and Chenopodiaceae are the dominant pollen types the geomorphology, archaeology and fossil faunal sequences of the terrestrial taxa. The vegetation has some representa- (see discussion in Field and Wroe, 2012; DeSantis et al., tion differences to the lower section with a much more 2017). Notably, contrary to the unsupported assertions of open aspect, and is probably chenopod shrubland. The Grun€ et al. (2010; see also Field et al., 2013), the rare earth aquatic taxa are dominated by Cyperaceae and Azolla,with element (REE) analysis has demonstrated that each horizon occasional Typha pollen, indicative of a shallow, still, examined in this study expressed internally consistent REE freshwater environment, is consistent with the clay-domi- patterns indicating that the bone assemblages in each horizon nated lacustrine environment, the formation of peds in are autochthonous and not of mixed age or origin (Trueman SU6B and fine plant roots that occur throughout the unit. et al., 2005). There is no evidence of reworking or fluvial activity (Field The bone-rich horizons of interest in this study are ca. 350– et al., 2008). Fungal spores are much more abundant in 400 ka in age apart and are separated by a stratified SU6 than the earlier part of the sequence (SU9). Sporor- sequence, in some places laminated, of silts and clays plus a miella values reach about 8% of the pollen sum but are consolidated hard-compacted (fragipan) layer (SU7). The generally <5%. Other fungal spores can be very abundant fragipan probably represents a stable surface that existed over in this section, reaching 40–50% of the pollen sum but a long period. The pollen/spore record from the lower layer with most values around 15–25%. (SU9) shows conditions that were more wooded than SU6A/ The pollen/spore record is in close agreement with the B, and while chenopod shrubland and open conditions previously published sequence (Field et al., 2002). The two predominated in each, it appears that the general environ- sections reflect different regional vegetation. The earlier ment was wetter in the lower unit.

Copyright # 2018 John Wiley & Sons, Ltd. J. Quaternary Sci., Vol. 33(4) 380–392 (2018) Copyright # 08Jh ie os Ltd. Sons, & Wiley John 2018

ae CUDDIE SPRINGS, NSW ubuliﬂor T m

ypha illarsia CasuarinaEucalyptusMelaleucaAcaciaDodonaeaGyrostemonaceaeGrevilleaHaloragusMalvaceaePolygonaceaePoaceae Asteraceae ChenopodiaceaeLamiaceaeCyperaceaeMyriophyllu T V Azolla Fungal spores Sporomiella Zone CONISS 110 115 SPORORMIELLA 120 SU6A 125 130 135 140

145 389 SEQUENCES FOSSIL AUSTRALIAN IN SPORES 150 155 SU6B 160 165 COMPACTED LAYER

Depth 170 SU7 175 180 SU8 185 190 SU9 195 200 205 210 215 220 20 20 20 20 40 20 20 40 60 80 20 40 246810 Total sum of squares .Qaenr c. o.3()3032(2018) 380–392 33(4) Vol. Sci., Quaternary J. Figure 7. Pollen and spore diagram for the Cuddie Springs sediments. The patterns of vegetation change are consistent with the original diagram (Field et al., 2002), with the addition of the Sporormiella spore sequence. Stratigraphic Unit 6 is composed of two units (6A and 6B) which formed under varying conditions and contain different assemblages with respect to one another. The grey dotted line marks the approximate boundary between A and B (Diagram: J. Dodson.) 390 JOURNAL OF QUATERNARY SCIENCE

Fungal spores were more abundant in SU6A/B, as were out the two faunal suites relative to Sporormiella abundance. spores of Sporormiella. Spores other than Sporormiella were It is likely that Sporormiella is associated with megaherbi- the most abundant. A Mann–Whitney U-test was applied to vores in Sahul, but it is also likely to be an indicator of extant Sporormiella percentages in the upper and lower sediment taxa such as Macropus, Dromaius and Vombatidae. In the sections (U ¼ 19.5, p < 0.05) and suggests mean Sporormiella SU9 level, Sporormiella is associated with a range of now- values were higher in SU6A/B. The good preservation of both extinct species. By contrast, an increase in Sporormiella in pollen and fungal spores thus suggests that dung may have SU6A/B occurs where both extant and extinct faunal species been relatively more abundant during deposition of the upper are common. It is the first time for Australia that Sporormiella section. One possibility is that standing water may have been can be linked to megaherbivores in context. What this record scarcer during the formation of the upper layer (acting as a does not do is provide evidence that megafauna dung alone waterhole), hence attracting both animals and humans to this harbours this particular fungus. We need more data on the locale. prevalence of Sporormiella in modern Australian species In using the suggested cut-off of >2% (following Feranec across the genus Macropus, as well as extant large avian et al., 2011; Gill et al., 2013) to indicate the presence of large species. At this point it is not scientifically balanced to claim herbivores, or perhaps large numbers of small herbivores, the that Sporormiella spores can tell us about megafauna, or their uppermost three samples (110–126 cm) and the samples at extinction in the Sahul context. 140 and 170, 185, 200 and 220 cm fall into this category. It is possible that the presence of large herbivores is not necessarily accompanied by Sporormiella spores in a fossil Acknowledgements. We are indebted to many people for supporting context in Australia. The earlier conclusion that the upper the work at Cuddie Springs: including the Green, Currey and Johnston unit was probably deposited in a time of freshwater scarcity families, Brewarrina Aboriginal Land Council, Phil Purcell (NPWS) and the Walgett Shire Council. The work was funded by the University (Field et al., 2008), as occurs at waterhole locales, is of New South Wales, the University of Sydney and the Australian consistent with these results. Conditions thus focused dung Research Council (DP0557923, LP0211430). We are grateful to the nearby, with Sporormiella also becoming more abundant and Australian Museum in Sydney for their support, especially Allison subsequently fossilized at the site. Dejanovic. Thanks also to Don Grayson, Adelle Coster and Emily Hull The taphonomy of Sporormiella representation is complex, for help along the way. and while there is a case for them being associated with megaherbivores, they are probably also associated with the Abbreviations. ESR, electron spin resonance; LGM, Last Glacial dung of other herbivores. Spore representation is not consis- Maximum; OSL, optically stimulated luminescence.. tent or may even be low or absent where megaherbivores are known to be present, probably due to the range of processes References such as source strength and transport systems which are Arenal F, Platas G, Pelaez F. 2007. A new endophytic species of responsible for their incorporation into sediments, as seen for Preussia (Sporormiaceae) inferred from morphological observations other fossils which can occur in sediment systems. and molecular phylogenetic analysis. Fungal Diversity 25: 1–17. Where does this leave the overall debate about the demise Atahan P, Dodson JR, Itzstein-Davey F. 2004. A fine-resolution of the Australian megafauna? Firstly, there remains a lack of Pliocene pollen and charcoal record from Yallalie, south-western data to be definitive about any single hypothesis. There are Australia. Journal of Biogeography 31: 199–205. few data on terminal dates of the animals themselves and the Baker AG, Bhagwat SA, Willis KJ. 2013. Do dung fungal spores make Signor–Lipps effect cannot account for species that have not a good proxy for past distribution of large herbivores? Quaternary Science Reviews 62: 21–31. been represented in the fossil record for tens of thousands of Basumatary SK, McDonald HG. 2017. Coprophilous fungi from dung years (see Wroe et al., 2013). 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