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Ethnographic accounts from around the world have reported the widespread use of insects as food by people1,2,3. In some cases, such as among the Shoshone and other Great Basin tribes of the U.S., swarms of grasshoppers and crickets were driven into pits and blankets4, while among the Paiute the larvae of Pandora moths (Coloradia pandora lindseyi) were smoked out of trees to fall into prepared trenches, where they would be cooked5. Across the world, insects could be mass-harvested, often seasonally, offering high nutritional value especially in fat, protein and vitamins6. The harvesting of insects in the past has ranged from opportunities to feed large communal gatherings during times of plenty, to more individualistic economic pursuits such as in the search for delicacies or the exploitation of low-ranked resources when other foods were scarce or depleted7,8,9. Irrespective of the catch, insects often represented an important component of the diet, and of the reliability and thus dependability of locales as resource zones, with implications for social scheduling and cultural practice. However, a paucity of archaeological studies of insect food remains has resulted in a downplay or omission of the use of insects from archaeological narratives and deep-time community histories10.
In Australia, a wide range of insects is known to have been eaten by Aboriginal groups, in particular the larvae (‘witchetty grubs’) of cossid moths (especially Endoxyla leucomochla) in arid and semi-arid areas11,12,13. Of particular interest to archaeologists and behavioural ecologists has been the seasonal consumption of Bogong moths by mass gatherings of Aboriginal groups in the southern portions of the Eastern Uplands14 (Fig. 1). However, no conclusive archaeological evidence has ever been reported for the processing or use of Bogong moths.
Figure 1

(A) Bogong moth, Agrotis infusa (photo: Ajay Narendra). (B) Thousands of moths per square metre aestivating on a rock surface (photo: Eric Warrant).

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The Cloggs Cave grindstone
Cloggs Cave is located 72 m above sea level in the southern foothills of the Australian Alps, in the lands of the Krauatungalung clan of the GunaiKurnai Aboriginal peoples of southeastern Australia (Fig. 2). The cave is a small, 12 m long × 5 m wide × 6.8 m high limestone karst formation that is today entered through a walk-through opening on the side of a cliff (Fig. 3). Indirect sunlight dimly illuminates the cave for much of the day (Supplementary Fig. S1).
Figure 2

Location of Cloggs Cave and the area of the GunaiKurnai Land and Waters Aboriginal Corporation, at the southern foothills of the Australian Alps. Esri ArcMap 10.5 (https://desktop.arcgis.com/en/arcmap/) and Adobe Illustrator CC 2017 (21.0) (https://helpx.adobe.com/au/illustrator/release-note/illustrator-cc-2017-21-0-release-notes.html) were used by CartoGIS Services, College of Asia and the Pacific at the Australian National University, to create the map.

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Figure 3

Cloggs Cave cliffline above the Buchan River flood plain, showing location of cave entrance (white rectangle) (photo: Bruno David).

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Archaeological excavations were first undertaken in 1971–197214, followed by a new program of excavations in 2019–2020, initiated by the GunaiKurnai Land and Waters Aboriginal Corporation and directed by Bruno David. The new excavations were aimed at better determining the site’s stratigraphy and the antiquity of Aboriginal occupation (Supplementary Fig. S2). An intensive dating programme showed that the oldest excavated evidence for human activity dates to between 19,330–19,730 cal BP (median age of 19,530 cal BP; cal BP = before AD1950) and 20,590–23,530 cal BP (median age of 21,690 cal BP) (all calibrated radiocarbon ages in the text are presented at 95.4% probability range. See “Methods”; Supplementary Fig. S3)15,16,17.
During the 2019 excavations, a small, flat grindstone was found. The finely stratified hearth layers of stratigraphic unit (SU) 2 in which it was found were radiocarbon-dated to 1567–1696 cal BP at their top (uncalibrated: 1724 ± 16 BP; median age of 1632 cal BP) and 2002–2117 cal BP at their base (uncalibrated: 2091 ± 16 BP; median age of 2062 cal BP). The grindstone therefore dates to between 1600 and 2100 years ago (see “Methods”; Supplementary Figs. S3 and S4)17. No other grindstone has been found at Cloggs Cave.
The grindstone is a tabular fragment of sandstone with two flat and parallel ground surfaces (Surfaces A and B), in the form of a flat dish (Fig. 4). It measures 10.5 cm long × 8.3 cm wide × 2.2 cm thick and weighs 304 g. The outer, intact margin is elliptical in plan view; the other three margins indicate old breaks that have been subsequently worn from use. Therefore, prior to its deposition at Cloggs Cave, the grindstone had been used in its current form.
Figure 4

The Cloggs Cave grindstone. (A) Surface A, with the accretion that formed across parts of the surface after its use. (B) Surface B. (C) Margin A. (D) Margin B. (E) Narrow end. The numbers in circles are the residue sample numbers; the ‘control’ samples are in areas where grinding did not take place (photos: Richard Fullagar).

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To understand how the grindstone was used, we undertook use-wear and residue analyses (see “Methods”). The central area of both its surfaces contain fine unidirectional striations (Supplementary Figs. S5A and S5B), a lowered but not levelled topography, and areas of missing or ripped quartz grains (Supplementary Figs. S5C and S5D). Its use to shape ground stone axes is an unlikely function because the Cloggs Cave grindstone surfaces are relatively flat with only very slight concavities, and the lowered surface topography (Fig. 4) lacks broad grooves typical of axe grinding.
When viewed at lower (up to 5 ×) magnification under a stereozoom microscope with a point source of light, each surface appears relatively rough compared with grindstones used for processing seeds, which, in Australia, tend to be highly smoothed and polished18,19. There are numerous ‘pits’ where sand grains have been plucked from the surface during use (Supplementary Fig. S5D). The presence of a lowered surface topography (Supplementary Fig. S5C) with a lack of smooth, developed polish suggests that the stone was not used to process siliceous plants.
The repeated mechanical action of grinding has been shown to force residues into the voids and interstitial spaces of ground surfaces, where they become trapped20,21,22. Residue analyses conducted on grindstones worldwide have relied on microscopic observations of individual residue morphologies. However, visually diagnostic features can be altered by the mechanical forces of grinding, heat, and contact with water and various environmental factors, which can cause residues to swell or become amorphous21,22,23,24. The distinctiveness of residue identifications can be enhanced significantly with the introduction of biochemical staining that can be observed under high-power microscopy and is best used in conjunction with microscopic use-wear analysis and identification of residue morphologies22.
We extracted nine samples, or ‘lifts’, for residue analysis from across Surface A and Surface B of the Cloggs Cave grindstone, including a control sample from an unworked part of each surface (Fig. 4; see “Methods”). These samples were analysed using a recently developed biochemical staining technique that enables residues to be identified from colorimetric changes occurring at a cellular level, rather than relying solely on structural features (see “Methods”)22. We used the collagen stain Picrosirius Red (PSR) to differentiate between plant and animal residues (see “Methods”). When PSR comes into contact with collagen (a protein unique to animals), it reacts to produce clear and distinctive staining and enhanced birefringence in cross-polarised light22,25.
Residues extracted from the grindstone
A range of residues were identified in the lifts, including amorphous collagen, collagen fibres, collagen structures, partially woven collagen, possible bone-like fragments, moth wing segments, a possible moth hind leg, amorphous cellulose, wood-like structures with pits, carbonised material, bordered pits and minerals (see below).
We found collagenous residues in mid-range densities across Samples 1 and 4 from Surface B and across Sample 5 from Surface A (Supplementary Fig. S6). These extractions were taken from central areas across each modified surface. In all cases, the frequency of the collagenous residues was approximately three times greater than the collagenous residues associated with the control samples. Residues include damaged collagen fibres of varying thicknesses, including some reticular fibres.
Woven collagen structures clearly show birefringence in cross-polarised light across Sample 1. Woven collagen, which forms quickly, is mechanically weak and usually associated with immature bone. Although woven collagen may persist as tendon and ligament attachments to bone, it is generally replaced by organised parallel collagen fibre bundles at skeleton maturity26. Collagen fibrils are found in the connective tissues of vertebrates as well as in invertebrates such as insects27, and may be present as individual strands, woven structures or parallel bundles, including among the Lepidoptera (moths and butterflies)28.
The density and combination of collagenous residues on the Cloggs Cave grindstone indicates that it was used to process fauna. A variety of collagenous materials (including woven collagen) were found in association with carbonised residues across Sample 2, which was extracted from a crystalline layer. The residues present on Samples 1 and 2 suggest that an insect or immature vertebrate was prepared and cooked using the grindstone.
We identified a moderate density of carbonised plant residues across Sample 2, in particular, wood-like structures with pits. These ranged from being partially to completely carbonised. Partially carbonised residues were also seen across Sample 4. In addition, bordered pits in small clusters were identified, along with pits within the carbonised structures. Bordered pits are cavities that are essential components in the water-transport system of higher-order plants and are found in the lignified cell walls of xylem conduits (vessels and tracheids). The pit membrane allows water to pass between xylem conduits, but limits the spread of embolism and vascular pathogens in the xylem29. Small quantities of lignin were also present (see “Methods”). Lignin is found in the cell walls of vascular plants (especially in wood and bark) and is responsible for the rigidity of plant structures.
The residues identified via biochemical staining are consistent with the use of twigs and bark as fuel for fires such as those of the microstratified ashy layers in which the grindstone was found (see Supplementary Fig. S3)17. Partially carbonised wood-like material was also noted across Sample 5. The density and distribution of carbonised residues varies across extractions. Our observations suggest either that: (a) the stone has been placed in or near fires; or (b) ash, embers or fires of varying heat were placed or lit across the stone, for varied durations of time.
We identified especially high densities (frequency of residue particles per unit volume of sample) of amorphous cellulose across Samples 1, 2, 4 and 5 (Supplementary Fig. S7). The presence of partially carbonised amorphous cellulose indicates that the plant residues were associated with fire. While the high density is indicative of a plant-processing event, there is no evidence of combinations of plant residues normally expected from plant processing. In particular, no starch grain or phytolith was seen in any of the extractions. While low heat can damage starch and cause its structure to be disrupted and its characteristic extinction-cross to be lost, low heat does not completely destroy starch visibility30. Similarly, phytoliths can be reshaped but not destroyed by fire31. The presence of animal and mineral residues but absence of starches and phytoliths is thus interpreted as a true absence of plant processing activities rather than a taphonomic effect of environmental factors negatively impacting their preservation.
We found a high density of variably carbonised insect wings in Sample 6 (Surface A), and lower densities in Samples 2 and 4. These wing fragments contain regular patterning or structure and exhibit distinct birefringence in cross-polarised light. A portion of proteinaceous material was associated with a ‘tangle’ of these structures (Fig. 5). To assess whether the insect remains were those of the Bogong moth, we compared the residues on Samples 2, 4 and 6 with a comparative reference sample (see “Methods”). All 26 cases of wing segments from the grindstone matched the metrical and morphological characteristics of those from Bogong moths in the reference material. The recorded damage on the archaeological wing segments, such as ripped wing structures, small rectangular wing fragments and tearing in various states of carbonisation, is what would be expected from ethnohistoric accounts of Bogong moth processing. Aboriginal people from across the region are known to have cooked Bogong moths on heated earth during the early and mid-nineteenth century. The moths were stirred during cooking, causing the wings and legs to be broken off by friction and heat. Some of the moths were pounded and ground into a paste which could then be smoked to preserve the food for weeks1,2.
Figure 5

Examples of Bogong moth segments from lifted samples (all at × 400 magnification). (A) Partially carbonised wing structures from Sample 2 (pp). (B) Partially carbonised wing structure and carbonised material from Sample 2 (pp). (C) Partially carbonised moth wing segment from Sample 4 (pp). (D–E) Damaged moth wing segment from Sample 6 (D pp; E xp). (F–G) Damaged moth wing segment from Sample 6 (F pp; G xp). (H) Damaged moth wing segment with proteinaceous material, from Sample 6 (pp). (I) Unburnt moth wing segment from Sample 4 (pp). (J) Damaged moth wing segment with attachment, from Sample 6 (pp). (K) Damaged moth wing segments from Sample 6 (pp). (L–M) Probable moth hind leg from Sample 6 (L pp; M xp). (N) Damaged moth wing segment from Sample 6 (pp). (O) Damaged moth wing segment with attachment, from Sample 6 (pp). Light source = plane (pp), part polarised (part pol) and cross-polarised (xp) (photos: Birgitta Stephenson).

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Though the time and place of the origin of this bloom is unknown, the presumable causes of it were high temperatures, abundant nutrients, low tidal amplitude, and little current. According to fishermen, these bioluminescent blooms were first seen about 15 nautical miles offshore of the Mandapam coast between India and Sri Lanka on 6th September, and subsequently moved towards the shore (Fig. 2). Bloom of N. scintillans in 2008 was reported to affect all the marine organisms including corals in GoM12. On 14th September, our preliminary assessment revealed that corals in Shingle and Krusadai islands were possibly affected by the bloom. A great multitude of N. scintillans cells were found settled on corals and other benthic organisms in the affected areas. A greenish settlement was observable on live coral colonies and other benthic organisms including macro algae, coralline algae and sponges etc.(Fig. S2). Settling of N. scintillans on benthic organisms has been reported to cause significant damage to the reef organisms through asphyxiation12. At Shingle Island, the area of significant impact was about 8.1 hectares on the shoreward side of the Island (79°14′14.38″E, 9°14′44.23″N) at depths between 1 and 3 m (Fig. 3). At Krusadai Island, an area of 2.1 hectares in the shoreward side was found affected by the bloom (79°13′20.78″E, 9°15′00.88″N) at depths between 1 and 2 m. The rest of the reef areas in both of these islands were healthy without any impact. The settled cells of N. scintillans were found to be washed ashore during subsequent surveys. In addition to dead fishes, a multitude of benthic communities such as crustaceans, mollusks and echinoderms were also found dead on the bottom in the impacted areas. Surveys between 15 and 18th September 2019 confirmed that corals in other islands (Pullivasal, Poomarichan, Manoliputti, Manoli and Hare) were in good health, and without any noticeable impact due to the bloom. Shingle and Krusadai islands occur closest to the mainland, and the concentrated bloom appeared to get trapped by currents between the mainland shore and islands.
Figure 2

(a) Green tide of Noctiluca scintillans in the Gulf of Mannar; (b) image of N.scintillans cells; size of the grid is 1 mm2 (N. scintillans exhibits bioluminescence when disturbed).

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Figure 3

Map showing the affected islands in the Mandapam group shown in Fig. 1. Base map was prepared by digitizing the georeferred Toposheet of Survey of India (http://www.surveyofindia.gov.in/) and field data using Open source GIS software (QGIS 3.10.6; https://qgis.org/en/site/forusers/download.html).

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On 14th September, coral mortality was not observed in the affected areas though the colonies were observed to be disturbed by the settling N. scintillans cells. Low dissolved oxygen levels have been reported to be the primary cause of benthic mortality during algal blooms22. Dissolved oxygen levels were 1.48 mg l−1 at Shingle Island and 2.02 mg l−1 at Krusadai Island in the affected areas. This compares to ‘normal’ levels for coral reefs of 5–8 mg l−1, and Haas et al.11 found that dissolved oxygen content less than 4 mg l−1 is detrimental to acroporid corals. Moreover, branching coral forms have been reported to be more susceptible to hypoxic episodes than spherical or massive forms5. Corals are routinely exposed to fluctuations in oxygen levels at the tissue level due to photosynthesis and respiration processes of endosymbionts7, but are negatively impacted when (sub-) lethal thresholds of hypoxia exposure are exceeded1,5,11. Lethal hypoxia thresholds appear to differ considerably between coral species, ranging between 0.5 and 4 mg O2 l−11,5,11, while sub-lethal hypoxia thresholds for corals are almost entirely unknown5.
Seawater temperature can significantly impact dissolved oxygen levels23,24. Water temperature was 29.9 and 29.8º C (Table 1) at Shingle and Krusadai islands respectively and these levels are marginally higher than the normal levels for this particular time of the year. Apart from the summer months (April to June), temperature levels in GoM do not go higher than 29º C20. The concentration of N. scintillans was 43.4 × 105 and 27.3 × 105 cells l−1 at Shingle and Krusadai Islands respectively; pH and TDS were also high in the affected area (Table 1). Dissolved oxygen levels in other sites of these two islands and in other five islands were higher than 5 mg l−1.
Table 1 Environmental characterization at the affected sites in Shingle and Krusadai Islands.
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During the next assessment on 17th of September 2019, severe coral mortality was observed at the affected sites. At Shingle Island, overall coral colony density was 134.25 (SE ± 3.28) no.100 m−2 (n = 537) within ten 20 m belt transects which is dominated by Acropora (64%) followed by Montipora (15%). Out of total 537 colonies, 33.52% (n = 180) were found dead (Fig. 4), which include 34.5 (SE ± 1.05) no.100 m−2 (n = 138) of Acropora, 7.75 (SE ± 0.75) no.100 m−2 (n = 31) of Montipora and 2.75 (SE ± 0.35) no.100 m−2 (n = 11) of Pocillopora. The death of coral colonies was so rapid that the coral tissue was intact on the colony surface and still had its natural colour (Fig. 5). When wafted with water by hand or with scuba air, the tissue peeled off exposing the skeleton (Supplementary video). Other observed genera such as Dipsastraea, Favites, Porites, Hydnophora, Goniastrea, Echinopora, Turbinaria, Platygyra, Goniopora and Symphyllia in the same site were all alive (Fig. S3), though with excess mucus production. This may be explained by differential lethal thresholds for oxygen levels at species and growth form levels5,19. At Krusadai Island, the overall coral density on 17th September was 66 (SE ± 2.54) no.100 m−2 (n = 132), dominated by Acropora. Among the counted colonies, 6 (SE ± 1.03) no.100 m−2 of Acropora were found recently dead while mortality was not observed in other available genera such as Montipora, Pocillopora, Dipsastraea, Favites, Porites and Turbinaria. Dissolved oxygen levels had increased to 3.78 mg l−1 at Shingle Island and to 4.02 mg l−1 at Krusadai Island at the affected sites and the water had started to become clear. The concentration of N. scintillans had reduced to 1.63 × 103 cells l−1 and 0.88 × 103 cells l−1 at Shingle and Krusadai Islands, respectively (Table 1).
Figure 4

Density of live and dead colonies of affected coral genera (Acropora, Montipora and Pocillopora) in Shingle Island, by date; the green line indicates the drastic decline of Acropora density between 17.09.2019 and 27.09.2019.

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Figure 5

Rapid mortality of corals presumably due to low oxygen levels caused by Noctiluca scintillans; (a, b) Acropora; (c) Montipora; (d) Pocillopora.

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Assessment on 27th September 2019 at the impacted area in Shingle Island, showed that the overall density of coral colonies within ten 20 m transects was 135.75 (SE ± 2.82) no.100 m−2 (n = 543) and of them 70.35% (n = 382) of colonies belonging to Acropora, Montipora and Pocillopora were found dead revealing that the impact of algal bloom was more severe than expected (Fig. 4). It was almost two weeks since the corals had died and hence secondary algae had started colonizing the dead colonies. On the same day at the impacted area of Krusadai Island, overall coral density within five belt transects was 65.5 (SE ± 1.83) no.100 m−2 (n = 131), of which 9.09% (n = 12) of colonies belonging to Acropora were found dead. By 27th September, dissolved oxygen levels had increased to 6.02 and 5.73 mg l−1 respectively at the affected areas of Shingle and Krusadai islands (Table 1). N. scintillans cells were absent in all the sites indicating the end of bloom. On 04th October 2019, the overall coral colony density within 20 m belt transects was 138 (SE ± 2.08) no.100 m−2 (n = 552) and of them 71.23% (n = 393) colonies belonging to Acropora, Montipora and Pocillopora were found dead at the area of impact in Shingle Island (Fig. 4). No further mortality was witnessed in the affected area of Krusadai Island. Secondary algae have completely overgrown the dead coral colonies making the reef look green (Fig. S4). Dissolved oxygen levels were reasonably high at 7.13 and 7.24 mg l−1 respectively at Shingle and Krusadai Islands during this time (Table 1).
Coral mortality due to algal bloom and consequent hypoxia has rarely been reported12,13,25. The present study reports that the impact of blooms can be severe on corals. Different coral species respond differently to low oxygen levels according to their respiration and photosynthesis5,26. Thus, low oxygen levels can orchestrate the coral mortality by affecting coral’s productivity and respiration7. Further, fast growing corals such as Acropora and Pocillopora have been reported to be more susceptible to low oxygen levels11,13,27. Fast growing coral species have faster metabolism rates28 and hence metabolic oxygen requirements are higher11,29. Thus, the mortality of fast growing species in the present study was presumably due to the low oxygen levels induced by N.scintillans bloom.
Bleaching episodes in 2010 and 2016 had also caused significant mortality to these fast growing species in GoM19,20. Corals in GoM start to bleach when water temperature exceeds 30º C and the temperature levels during this bloom period ranged between 28.4 and 29.9º C. Though bleaching was not observed, heat stress might also have played its role in coral mortality along with low oxygen levels as the temperature level almost reached 30º C. Similar temperature levels were reported during the bloom of N. scintillans in 2008 in GoM12.
Corals in Gulf of Mannnar are still recovering from the 2016 bleaching episode20 and hence the present decline is significant. Phase shifts on coral reefs are predominantly associated with shifts from hard coral-dominated communities to macroalgae-dominated ones30. Space competition between corals and other organisms such as algae and sponges has been reported to negatively impact the corals of GoM after the 2016 bleaching event20,31. At present, secondary algae have completely occupied the dead coral colonies, which will affect the coral recovery by hindering the attachment of new coral recruits during the next spawning season32. Recent studies suggest hypoxia increases coral susceptibility to bleaching27, and may increase disease prevalence and algal proliferation7. Thus algal blooms add to the existing array of threats to corals of GoM that needs to be understood more with further focused research.
On account of the problems related to climate change, there has been a steady and severe decline of coral reefs in the past two decades. Bleaching and diseases have been reported to cause mass coral mortalities within a very short time. The observations of the present study alert us to possible mass mortality due to short-term hypoxic condition caused by algal blooms. Algal blooms and hypoxic conditions are predicted to occur more frequently in the future due to climate change14. Hence, it is likely that shallow water coral reefs will be affected more frequently by temporary low oxygen levels caused by algal blooms. More studies are, however, required to understand the mechanism of coral mortality due to algal blooms, impacts on community composition and the potential for subsequent recovery. More

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