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    An example of DNA methylation as a means to quantify stress in wildlife using killer whales

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    Field measurements of a massive Porites coral at Goolboodi (Orpheus Island), Great Barrier Reef

    The location, diameter, height and circumference of the coral were measured (Table 1, Fig. 2). The Porites was brown to cream in colour and hemispherical in shape (Fig. 2). It was identified as either Porites lutea (Hump or Pore coral) or P. lobata (Lobe coral)14.The primary habitat on the Porites was live coral (70%), followed by sponge, live coral rock and a small amount of macroalgae (Table 2). No recently dead coral, coral rubble or sand was recorded (Table 2). We observed competition between the Porites and other species of coral and invertebrate including encrusting sponge, plating and branching Acropora spp., Montipora, Chlorodesmis, soft coral and zoanthids (Table 2, Figs. 3, 4).Table 2 Reef Health Impact Survey (RHIS) of habitat and species categories on Porites sp.Full size tableFigure 3Detail of the sub-habitats and competitive interactions Porites sp. and boring sponge Cliona viridis (left) and live coral Porites sp. and Montipora sp. (right) along interspecific contact zones.Full size imageFigure 4Detail of Reef Health Impact Survey (RHIS) of Porites.Full size imageThe boring sponge, Cliona viridis, is abundant on the Great Barrier Reef15. It is a common bioeroding species advancing laterally at around 1 cm and to a depth of 1.2 cm per annum15. Abundance of Cliona viridis is often correlated to substrate availability and water energy with the greatest abundance often on the windward side of bommies15. This correlates to our observations as the large proportion of the substrate estimated to cover the bommie (15%) was on the windward side. The sponge’s advances will likely continue to compromise the colony size and health.We recorded marine debris at the base of the Porites. The debris was 2–3 m of rope that appeared to have been wrapped around the base of an adjacent coral. Adjacent to the bommie were three concrete blocks.How big is the Porites coral at Goolboodi compared to other big corals in the GBR, and the world? Potts et al.6 reported a very large, rounded Porites colony, 6.9 m in diameter which is 3.1 m smaller than this study. Lough et al.16 reported coral cores from colonies between 1.6–8.0 m in height with the largest corals of 6.0 m at Havannah, North Molle and Masthead Islands, 7.5 m at Abraham Reef and 8.0 m at Sanctuary Reef. Recognising the limitations of published data, the Porites coral at Goolboodi is the largest diameter coral that has been measured, and the 6th tallest in the GBR. It is unknown if the other corals are still alive or dead.Other comparatively large massive Porites have previously been located throughout the Pacific. These have included multiple bommies measuring more than 10 m4 and one exceptionally large colony observed measuring 17 m × 12 m in American Samoa17. Additionally, large Porites sp. bommies have been observed at Green Island, 30 km east of Taiwan18 as well as an 11 m diameter Porites australiensis at Sesoko Island, Okinawa, Japan19.How old is this massive Porites? In discussions with the Australian Institute of Marine Science (AIMS), there is a robust, linear relationship ( > 80% variance explained) between Porites average linear extension rate and average annual sea surface temperature (SST)20,21 that provides an estimate of colony age from its height. Using average annual SST at 18.5S, 146.5E of 26.12C (from HadiSST data set), the estimated linear extension rate is determined by (2.97 × 26.12) − 65.46 = 1.21 cm/year. Given the colony height of 5.1–5.3 m, this gives an estimated age of 421–438 years. This is well before European exploration and settlement of Australia. AIMS has investigated over 328 colonies of massive Porites corals from 69 reefs along the GBR and has aged them as being from 10–436 years21. AIMS has not investigated this coral (pers. comm Neal Cantin). Based on limitations of published data, the Porites coral at Goolboodi is one of the oldest corals on the GBR.Why is the Porites partially dead on top and living on the side? The proportion of live coral tissue on a colony reflects the cumulative, integrated effect of both beneficial and adverse environmental factors. Substantial portions of coral tissue can die from exposure to sun at low tides or warm water without lethal consequences to the colony as a whole10. Partial mortality of large bommies provides available real estate for opportunistic, fast growing sessile organisms. In this instance, multiple species of tabulate and branching Acropora sp., encrusting Montipora sp. and encrusting sponges are among the benthic organisms to have colonised 30% of the coral bommies’ surface area. Intraspecific competition is also evident from the skeletal barriers created along contact zones22 (Fig. 3). There was no observation of disease or coral bleaching.The Porites is located in a relatively remote, rarely visited and highly protected Marine National Park (green) zone. Its location had not been previously reported and there is no existing database for significant corals in Australia or globally. Cataloguing the location of massive and long-lived corals can have multiple benefits. Scientific benefits include geochemical and isotopic analyses in coral skeletal cores which can help understand century-scale changes in oceanographic events and can be used to verify climate models. Social and economic benefits can include diving tourism, citizen science23 culture and stewardship. Perhaps the Significant Trees Register, which was designed by the National Trust24 to protect and celebrate Australia’s heritage could be considered as a model. There are risks of cataloguing the location of massive corals. It could be damaged by direct and indirect human uses including anchoring, research and pollution.Indigenous languages are an integral part of Indigenous culture, spirituality, and connection to country. We consulted Manbarra Traditional Owners about protocol and an appropriate cultural name for the Porites and they considered: Big (Muga), Home (Wanga), Coral reef (Muugar), Coral (Dhambi), Old (Anki, Gurgu), Old man (Gulula) and Old person (Gurgurbu)25. The recommendation by Manbarra Traditional Owners is that the Porites is named as Muga dhambi (Big coral). The feedback from the process of consultation was very positive with acknowledgement of the respect that the scientists have demonstrated to acknowledge Traditional Owners in this way.The large Porites coral at Goolboodi (Orpheus) Island is unusually rare and resilient. It has survived coral bleaching, invasive species, cyclones, severely low tides and human activities for almost 500 years. In an attempt to contextualise the resilience of these individual Porites we have reviewed major historic disturbances such as coral bleaching which has occurred since at least 1575 and potentially 99 bleaching events in the GBR over the past 400 plus years26. Other indicators such as high-density ‘stress bands’ were recorded from 1877 and are significantly more frequent in the late twentieth and early twenty-first centuries in accordance with rising temperatures from anthropogenic global warming27. In addition there have been an average of 1–2 tropical cyclones per decade (40–80 in total) that have potentially impacted the coral adjacent to Goolboodi Island28,29; 46 tropical cyclones impacted the area between Ingham and Townsville from 1858 to 200830. The cumulative impact of almost 100 bleaching events and up to 80 major cyclones over a period of four centuries, plus declining nearshore water quality contextualise the high resilience of this Porites coral. Looking to the future there is real concern for corals in the GBR due to many impacts including climate change, declining water quality, overfishing and coastal development31,32. This field note provides important geospatial, environmental, and cultural information of a rare coral that can be monitored, appreciated, potentially restored and hopefully inspire future generations to care more for our reefs and culture. More

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    Methane from microbial hydrogenolysis of sediment organic matter before the Great Oxidation Event

    Model A: abundances and δ13C of short alkanesConsidering the cleavage at position m (between the no. m and no. m + 1 carbon atoms) of an n-alkyl chain with n carbon atoms (1 ≤ m 15), the isotopic compositions of gas products are insensitive to the initial kerogen side chain length distribution. For initial values, a δ13C value of −35‰ is applied. The initial chain length is in a normal distribution with a peak of C17 and a standard deviation of σ = 2 carbon atoms. The initial alkane concentrations are assumed to be 0.For simplicity, we assume that since there is no isotopic fractionation within or between the alkyl chains at the beginning of hydrogenolysis, the probability of 13C substitution at any position of any side chain is identical and determined by the initial carbon isotopic composition δ13C. Multiple 13C substitutions on a C–C chain are omitted because consideration of multiple substitutions would drastically increase the modelling complexity. This approximation is valid when the C–C chain is not too long. For example, the ratio between the probabilities of double and single 13C substitution in a C20 chain is ({left[{left(begin{array}{c}20\ 2end{array}right)}{{left(frac{{,}^{13}{{{{{rm{C}}}}}}}{{,}^{12}{{{{{rm{C}}}}}}}right)}}^{2}right]}/{left[{left(begin{array}{c}20\ 1end{array}right)}{left(frac{{,}^{13}{{{{{rm{C}}}}}}}{{,}^{12}{{{{{rm{C}}}}}}}right)}right]}) ≈ 10% for 13C/12C ~ 0.01. Such a chain is long enough that the δ13C of gas products is insensitive to C–C chain length. Numerical simulation was conducted with Mathworks MATLAB 2020a.Model B: bulk and clumped isotopic fractionations of CH4
    Conversion of methylene in a long C–C chain to methane is generalised into two steps:$${{{{{rm{R}}}}}}{mbox{-}}{{{{{{rm{CH}}}}}}}_{2}{mbox{-}}{{{{{rm{R}}}}}}{^prime} mathop{longrightarrow}limits^{{{{{{{rm{r}}}}}}}_{a}}_{+{{{{{rm{H}}}}}}}{{{{{rm{R}}}}}}{mbox{-}}{{{{{{rm{CH}}}}}}}_{3}mathop{longrightarrow}limits^{{{{{{{rm{r}}}}}}}_{b}}_{+{{{{{rm{H}}}}}}}{{{{{{rm{CH}}}}}}}_{4}$$
    (8)
    The first step (step a) is the conversion of the methylene group R-CH2-R′ to a methyl group (RCH3) by accepting a capping hydrogen atom from the hydrogen donor (activated H2); the second step (step b) is the conversion of the methyl group to methane by accepting another capping hydrogen atom. This scheme is highly generalised, and each step may involve multiple elementary biochemical reaction steps, such as the binding of H2 and long alkyl chains to the enzyme, activation of H–H and C–C bonds, and release of the short alkane products from the enzyme. It is beyond the scope of this work to discuss the detailed biochemical reaction steps. But the cleavage and formation of chemical bonds in these steps should be constrained by the observed isotopic patterns.Due to the computational complexity, we did not use the random scission model (Model A) in the simulation involving clumped isotopic fractionation, as explained in the following. A conventional kinetic model of the decomposition of organic matter without considering the constraints of C–C chain lengths is a zero-dimensional problem. Modelling the random cutting of long C–C chains without considering isotopes is a one-dimensional problem, and modelling bulk carbon isotopic fractionation during random cutting (Model A) is a two-dimensional problem. If 13C–13C coupling is included in random cutting, the modelling is a three-dimensional problem; a complex Monte Carlo method has been applied to deal with this problem19. If the 13C–D or D–D coupling is included in Model B, as we wish, it is a problem above the fourth dimension. The complexity of programming and the difficulty of computation make the model unattainable; even if it is achievable, solving this problem is far beyond the scope of this work.Reaction equation Eq. 8 is expanded to the scheme in Fig. 3a to quantify the five most abundant isotopologues in methane (three or more substitutions such as 13CH2D2 or 12CHD3 are ignored due to their low abundances). For the subscripts in Fig. 3a (m, i, and j in ramij or rbmij), the first digit (m = 0 or 1) is the number of 13C atoms involved in the reaction, the second digit (i = 0, 1, or 2) is the number of deuterium atoms connected in the methylene or methyl group, and the third digit (j = 0 or 1) is the number of deuterium atoms in the hydrogen donor.Clumped isotopic compositions of methylene and methane are defined as the following:$$left{begin{array}{l}{{Delta}} {{{{{rm{R}}}}}}{,}^{13}{{{{{rm{C}}}}}}{{{{{rm{HDR}}}}}}^{prime} =frac{({{{{{rm{R}}}}}}{,}^{13}{{{{{rm{C}}}}}}{{{{{rm{HDR}}}}}}^{prime} )({{{{{rm{R}}}}}}{,}^{12}{{{{{rm{C}}}}}}{{{{{{rm{H}}}}}}}_{2}{{{{{rm{R}}}}}}^{prime} )}{({{{{{rm{R}}}}}}{,}^{13}{{{{{rm{C}}}}}}{{{{{{rm{H}}}}}}}_{2}{{{{{rm{R}}}}}}^{prime} )({{{{{rm{R}}}}}}{,}^{12}{{{{{rm{C}}}}}}{{{{{rm{HDR}}}}}}^{prime} )}-1hfill\ {{Delta}} {{{{{rm{R}}}}}}{,}^{12}{{{{{rm{C}}}}}}{{{{{{rm{D}}}}}}}_{2}{{{{{rm{R}}}}}}^{prime} =4frac{({{{{{rm{R}}}}}}{,}^{12}{{{{{rm{C}}}}}}{{{{{{rm{D}}}}}}}_{2}{{{{{rm{R}}}}}}^{prime} )({{{{{rm{R}}}}}}{,}^{12}{{{{{rm{C}}}}}}{{{{{{rm{H}}}}}}}_{2}{{{{{rm{R}}}}}}^{prime} )}{{({{{{{rm{R}}}}}}{,}^{12}{{{{{rm{C}}}}}}{{{{{rm{HDR}}}}}}^{prime} )}^{2}}-1hfill\ {{Delta}} {,}^{13}{{{{{rm{C}}}}}}{{{{{{rm{H}}}}}}}_{3}{{{{{rm{D}}}}}}=frac{({,}^{13}{{{{{rm{C}}}}}}{{{{{{rm{H}}}}}}}_{3}{{{{{rm{D}}}}}})({,}^{12}{{{{{rm{C}}}}}}{{{{{{rm{H}}}}}}}_{4})}{({,}^{12}{{{{{rm{C}}}}}}{{{{{{rm{H}}}}}}}_{3}{{{{{rm{D}}}}}})({,}^{13}{{{{{rm{C}}}}}}{{{{{{rm{H}}}}}}}_{4})}-1hfill\ {{Delta}} {,}^{12}{{{{{rm{C}}}}}}{{{{{{rm{H}}}}}}}_{2}{{{{{{rm{D}}}}}}}_{2}=frac{8}{3} frac{({,}^{12}{{{{{rm{C}}}}}}{{{{{{rm{H}}}}}}}_{2}{{{{{{rm{D}}}}}}}_{2})({,}^{12}{{{{{rm{C}}}}}}{{{{{{rm{H}}}}}}}_{4})}{{({,}^{12}{{{{{rm{C}}}}}}{{{{{{rm{H}}}}}}}_{3}{{{{{rm{D}}}}}})}^{2}}-1 hfillend{array}right.$$
    (9)
    Note that the isotopic compositions here are expressed in decimals; they should be multiplied by 1000 to give per mil values.The deuterium isotope ratio between the hydrogen donor (denoted with subscript B) and the methylene group (subscript A) is expressed as:$${alpha }_{{{{{{rm{A}}}}}}}^{{{{{{rm{B}}}}}}}=frac{1+{{{delta }}{{{{{rm{D}}}}}}}_{{{{{{rm{B}}}}}}}}{1+{{{delta }}{{{{{rm{D}}}}}}}_{{{{{{rm{A}}}}}}}}$$
    (10)
    For each reaction step in Fig. 3a, the corresponding rate constants are denoted as kamij for step a or kbmij for step b. Kinetic fractionation factors αkamij = kamij/ka000 and αkbmij = kbmij/kb000 define KIEs. Note that a DKIE is often expressed as kH/kD, which is the reciprocal of the αk nomenclature here. A DKIE may be primary or secondary; a primary DKIE results in αka001 ≠ 1 and αkb001 ≠ 1, and a secondary one results in αka010 ≠ 1 and αkb010 ≠ 1. Kinetic clumped isotope fractionation factors γamij = αkamij/(αka100mαka010iαka001j) and γbmij = αkbmij/ (αkb100mαkb010iαkb001j) define the excessive KIE due to isotope clumping in steps a and b, respectively30.Conversion of the reactant R-CH2-R′ is defined as 1 − f, where f is the residual fraction of R-CH2-R′:$$f=({{{{{rm{R}}}}}}{mbox{-}}{{{{{{rm{CH}}}}}}}_{2}{mbox{-}}{{{{{rm{R}}}}}}{^prime} )/{({{{{{rm{R}}}}}}{mbox{-}}{{{{{{rm{CH}}}}}}}_{2}{mbox{-}}{{rm{R}}}{^prime} )}_{{{{{{rm{initial}}}}}}}$$
    (11)
    Considering the isotope abundance of D  1 or γb011  > 1, as shown by the Δ12CH2D2 expression in Eq. (13). With this prerequisite, either an inverse primary DKIE (1° DKIE, αka001  > 1, αkb001  > 1) or an inverse secondary DKIE (2° DKIE, αka010  > 1, αkb010  > 1) is necessary, and through numerical simulation, we found that only the inverse 1° DKIE satisfies the above-mentioned δDA, δDB, and Δ12CH2D2 values.Two scenarios (one is the pure stochastic condition, the other is with an inverse 1° DKIE) are modelled (Fig. 3). The parameters are listed in Table 1. For comparison, analytical solutions at the beginning and end of reactions from Eqs. (12) and (13) are presented. The numerical and analytical solutions are nearly identical at the beginning of conversion. There are small differences between the numerical and analytical solutions at the endpoint because the abundance of the hydrogen donor is not extremely excessive. A weak 13C fractionation between the organic precursor and the methane product is obtained with the KIE parameters (Fig. 3b). With such a weak 13C KIE, Δ13CH3D is nearly constant for reaction extent (Fig. 3c). Note that we applied an inverse 13C KIE, as required by the δ13C distribution of the alkane gases (Method 1, Model A). The δD and Δ12CH2D2 values are independent of 13C KIE. Both the bulk and clumped isotopic compositions of methane within the range of reported values are obtained at the organic precursor conversion of 0.65–0.70 as constrained by Fig. 2. More

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