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    Cleaner fish are sensitive to what their partners can and cannot see

    Our measure of interest was whether females ate more of the flake items (i.e., cheated less quickly) when the male had perceptual access than when he did not. Consistent with our predictions, females ate fewer flake items in the male not visible condition (Mean = 3.6 items, SD = 3.2) than in the male visible condition (Mean = 4.5, SD = 3.1; Fig. 2A; for flake items eaten by pairs see Supplementary Fig. S1). Additionally, females tended to cheat less over rounds (Supplementary Fig. S2). Indeed, the number of flake items eaten was predicted by both conditions (LRT, X21 = 8.13, p = 0.004; Fig. 2A; Supplementary Table S1) and round (LRT, X21 = 12.46, p  More

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    Use of timelapse photography to determine flower opening time and pattern in banana (Musa spp.) for efficient hand pollination

    In banana, bract opening behavior depends on the time of the day, the position of the bract, and sex of the flowers enclosed by the bract. Bract opening is a continuous process especially in the first bracts subtending female flowers of some genotypes; it starts in the evening and continues through the night (Table 1). In cases where bracts did not fully open, the process was halted early morning and resumed in the evening. It is therefore not obvious to judge whether such bracts have opened or not. However, opening is permanent as opposed to some plant species which open and close their flowers at specific times. Ssebuliba et al.16 considered East African Highland bananas ready for pollination when bracts were half way open with stigmas having a creamy white appearance. According to observations made in the current study, it can be said that bract lifting is indicative of flower opening thus pollination can start.Bract lift and bract roll seemed to be a response of a certain light quality6, the response time and speed are genotype dependent. Finger curling also seems to be triggered by the same factors that lead to bract opening. Bract opening and finger curling are likely to be a response of changes in turgor pressures in cells that lead to tissues being pushed in a given direction17. This was evident with upward movement of the inflorescence from the horizontal-pendent toward the horizontal position in the evening and downward movement towards the pendent position by mid-morning. These movements were genotype dependent and small, maximum oscillation was about 10˚. A similar pattern was observed for leaf folding to influence relative canopy cover18.Generally, bracts subtending female flower lifted and started rolling earlier than those subtending male flowers. However, male flowers ended opening before female flowers, resulting in faster bract opening for male flowers (Table 1 and t-test). This might be due to the smaller bract size of male flowers (Fig. 1) or an adaption for female flowers to find male flowers open with ready pollen. Consequently, the strategy ensures maximum pollination success and survival of the Musa spp. Studies have revealed that pollen viability reduces with time after flower opening1. This is in agreement that controlled pollination should be done between 07:00 and 10:00 h7. In comparison to lilies, some flowers were observed also to open starting at 17:00 h while others open during day. Both nocturnal and diurnal pollinators were found to be active flower visitors19. This implies that pollination in banana can start in the evening as long as bracts for parents in the cross of interest lift in time.In Musa itinerans, two nectar production peaks were found, that is between 08:00 to 12:00 h and 20:00 to 24:00 h20. This maybe a close depiction of what happens in edible bananas thus emphasizing the potential importance of diurnal and nocturnal pollinators. Bats, bees, and birds were found to be among the most important pollinators of bananas at Onne, Nigeria10. However, natural pollinators were not the main focus of the study though they are good indicators of when stigmas might be highly receptive. Since nectar quality and quantity varies between different agro-ecologies and seasons21, flower visitations and seed set are also expected to vary accordingly. Different agro-ecologies are also expected to experience variable BOTs due to variable solar radiation. Likewise the different growing seasons (rainy and dry) might also affect BOTs and therefore seed set22. However, a comparison of time from sunrise to beginning of bract lift of Musa AAA Cavendish cultivars in a glasshouse and M. basjoo in the garden in Belgium revealed no significant difference6. But comparison of bract curling time in Mchare in Arusha with short days and Cavendish cultivars in a glasshouse in Belgium with long days in summer, there was early curling in the glasshouse. However, bract lift time may be a better event to use for comparison than bract curling or rolling time.Bracts of both female and male flowers of different genotypes completed opening at different times and this may be partly the reason for variable pollen viability and stigma receptivity (Table 1). Female flowers that finish opening much earlier may set less seed compared to those that finish opening closer to the routine time of hand pollination between 07:00 and 10:00 h. Conversely, male flowers that are ready shortly before the time of hand pollination are expected to have higher pollen viability. This probably explains the high fertility of ‘Calcutta 4’ as it finished opening at 06:30 h. Some male flowers like those of Matooke finished opening as early as 21:54 h (Table 1) and are expected to have pollen with low viability at the time it is measured the next day.All observed inflorescences opened one female bract on the first day, increasing to multiple bracts opening on subsequent days (Fig. 2). One to three bracts subtending female flowers were observed to open per day from the second bract position of the inflorescence. The pattern of opening took on a hyperbolic shape with up to four bracts opening on the fourth day in the midsection of the inflorescence. For hand pollination, more clusters are therefore expected to be pollinated per day during bract opening in the mid-section of the inflorescence. The different clusters of female flowers that open on the same day are likely to have stigmas with varying receptivity. The darker appearance of stigmas of former clusters compared to creamy stigmas in latter clusters reflects higher receptivity in the latter2. This may explain why some clusters set more seed especially in the mid-section of a seemingly fertile inflorescence.Upon complete opening of female and transitional bracts, inflorescences went into a pause period before male flowers opened (Table 2). In additional to spatial separation of flowers, this is temporal separation to promote cross pollination in banana. However, temporal separation of male and female flowers is not very effective for genotypes that had less than 24 h of separation. With aid of crawling insects, self-pollination may happen between the last female cluster and the first male cluster as stigmas are likely to be receptive for more than one day. Once male flowers started opening, one bract opened per day and occasionally two bracts were observed to open on the same day. For highly fertile genotypes like ‘Calcutta 4’, ample pollen is produced to pollinate many female flowers. Male flowers are also produced throughout the inflorescence growth period which ensures constant supply of pollen especially for controlled hand pollination. Averages of bracts subtending male flowers opening per day could not be calculated as there were two to three observed bracts subtending male flowers for most genotypes.It appears that proximal bracts subtending female flowers are less stimulated to lift and roll compared to distal bracts subtending female flowers and all bracts subtending male flowers. This was revealed by low vigour of bract lift and the small angle of lift at 08:00 h especially in the first female flower cluster (Figs. 2, 3). The bract angle of lift increases from proximal to distal end and this has been linked to reduced fertility in proximal clusters2. But it may not be the case since highly female (in all clusters) and male fertile ‘Calcutta 4’ showed the same pattern as edible bananas. The high R2 for female bract roll scores compared to bracts subtending male flowers was a result of more bracts used to calculate averages for bracts subtending female flowers compared to bracts subtending male flowers (Fig. 3). For bracts subtending male flowers, two to three bracts were observed for most genotypes thus the first three data points were close to the trend line. Since the number of female clusters varies, reducing number of data points were used to calculate average bract lift angles in the distal end or larger inflorescences. Besides, bract lift angles of some clusters could not be measured because of obscurity or being in awkward positions. This led to the last two points being far off the trend line for angle of lift and hence a low R2.Flower opening time is said to be genetically and environmentally controlled, results from this study are in agreement since light had considerable influence on bract opening events (Tables 1, 3). Significant effects of temperature, solar radiation, and vapor pressure deficit on flower opening time have been observed in rice11. For Musa spp., only light has a significant relationship with BOT. However, there was early curling under long summer days in the glasshouse in Belgium compared to short days in Arusha field conditions6. This suggested a particular light signal for BOT in Musa spp. It is unclear why high light intensity led to early lift of bracts subtending male flowers and this calls for farther investigation. Since bracts subtending male flowers instinctively open later than bracts subtending female flowers, light intensity had less effect on the former bracts. The small sample size could have also had an impact on the results in the study, the light flush from the camera could have also affected the results. The extent of weather effects on BOT in banana need to be studied in field conditions of locations with significantly different day length for a more reliable conclusion. More

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    Effect of host switching simulation on the fitness of the gregarious parasitoid Anaphes flavipes from a novel two-generation approach

    1.Hairston, N. G., Smith, F. E. & Lawrence, B. S. Community structure, population control, and competition. Am. Nat. 94, 421–425 (1960).Article 

    Google Scholar 
    2.Gross, P. Insect behavioral and morphological defenses against parasitoid. Annu. Rev. Entomol. 38, 251–273 (1993).Article 

    Google Scholar 
    3.Tylikinais, J. M., Tscharntke, T. & Klein, A. M. Diversity, ecosystem function and stability of parasitoid—host interactions across a tropical habitat gradient. Ecology 87, 3047–3057 (2006).Article 

    Google Scholar 
    4.Strand, M. R. & Obrycki, J. J. Host specificity of insect parasitoids and predators. Bioscience 46, 422–429 (1996).Article 

    Google Scholar 
    5.Dawkins, R. & Krebs, J. R. Arms races between and within species. Proc. R. Soc. Lond. B. 205, 489–511 (1979).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    6.Kraaijeveld, A. R., van Alphen, J. J. M. & Godfray, H. C. J. The coevolution of host resistance and parasitoid virulence. Parasitology 116, 29–45 (1998).Article 

    Google Scholar 
    7.Jeffries, M. J. & Lawton, J. H. Enemy free space and the structure of ecological communities. Biol. J. Linn. Soc. 23, 269–286 (1984).Article 

    Google Scholar 
    8.Grosman, A. H. et al. No adaptation of a herbivore to a novel host but loss of adaptation to its native host. Sci. Rep.-UK 5, 16211 (2015).ADS 
    CAS 
    Article 

    Google Scholar 
    9.Diamond, S. E. & Kingsolver, J. G. Fitness consequences of host plant choice: A field experiment. Oikos 119, 542–550 (2010).Article 

    Google Scholar 
    10.Meijer, K., Schilthuizen, M., Beukeboom, L. & Smit, C. A review and meta-analysis of the enemy release hypothesis in plant–herbivorous insect systems. PeerJ 4, e2778 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    11.Forbes, A. A., Powell, T. H., Stelinski, L. L., Smith, J. J. & Feder, J. L. Sequential sympatric speciation across trophic levels. Science 323, 776–779 (2009).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    12.Grosman, A. H., Holtz, A. M., Pallini, A., Sabelis, M. W. & Janssen, A. Parasitoids follow herbivorous insects to a novel host plant, generalist predators less so. Entomol. Exp. Appl. 162, 261–271 (2017).Article 

    Google Scholar 
    13.Soler, R., Bezemer, T. M., Van Der Putten, W. H., Vet, L. E. & Harvey, J. A. Root herbivore effects on above-ground herbivore, parasitoid and hyperparasitoid performance via changes in plant quality. J. Anim. Ecol. 74, 1121–1130 (2005).Article 

    Google Scholar 
    14.Ode, P. J. Plant chemistry and natural enemy fitness: Effects on herbivore and natural enemy interactions. Annu. Rev. Entomol. 51, 163–185 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    15.Thompson, J. N. Trade-offs in larval performance on normal and novel hosts. Entomol. Exp. Appl. 80, 133–139 (1996).Article 

    Google Scholar 
    16.Lucas, É., Coderre, D. & Brodeur, J. Intraguild predation among aphid predators: Characterization and influence of extraguild prey density. Ecology 79, 1084–1092 (1998).Article 

    Google Scholar 
    17.Henry, L. M., May, N., Acheampong, S., Gillespie, D. R. & Roitberg, B. D. Host-adapted parasitoids in biological control: Does source matter?. Ecol. Appl. 20, 242–250 (2010).PubMed 
    Article 

    Google Scholar 
    18.Mackauer, M. Sexual size dimorphism in solitary parasitoid wasps: influence of host quality. Oikos 76, 265–272 (1996).Article 

    Google Scholar 
    19.Bezemer, T. M. & Mills, N. J. Clutch size decisions of a gregarious parasitoid under laboratory and feld conditions. Anim. Behav. 66, 1119–1128 (2003).Article 

    Google Scholar 
    20.Samková, A., Hadrava, J., Skuhrovec, J. & Janšta, P. Host population density and presence of predators as key factors influencing the number of gregarious parasitoid Anaphes flavipes offspring. Sci. Rep.-UK 9, 6081 (2019).ADS 
    Article 
    CAS 

    Google Scholar 
    21.Schmidt, J. M. & Smith, J. J. B. Correlations between body angles and substrate curvature in the parasitoid wasp Trichogramma minutum: a possible mechanism of host radius measurement. J. Exp. Biol. 125, 271–285 (1986).Article 

    Google Scholar 
    22.Boivin, G. & Baaren, J. The role of larval aggression and mobility in the transition between solitary and gregarious development in parasitoid wasps. Ecol. Lett. 3, 469–474 (2000).Article 

    Google Scholar 
    23.Mayhew, P. J. The evolution of gregariousness in parasitoid wasps. P. Roy. Soc. Lond. B. Bio. 265, 383–389 (1998).Article 

    Google Scholar 
    24.Pexton, J. J. & Mayhew, P. J. Competitive interactions between parasitoid larvae and the evolution of gregarious development. Oecologia 141, 179–190 (2004).ADS 
    PubMed 
    Article 

    Google Scholar 
    25.Harvey, P. H. & Partridge, L. Murderous mandibles and black holes in hymenopteran wasps. Nature 326, 128–129 (1987).ADS 
    Article 

    Google Scholar 
    26.Godfray, H. C. J. The evolution of clutch size in parasitic wasps. Am. Nat. 129, 221–233 (1987).Article 

    Google Scholar 
    27.Rosenheim, J. A. Single-sex broods and the evolution of nonsiblicidal parasitoid wasps. Am. Nat. 141, 90–104 (1993).Article 

    Google Scholar 
    28.Mayhew, P. J. & van Alphen, J. J. Gregarious development in alysiine parasitoids evolved through a reduction in larval aggression. Anim. Behav. 58, 131–141 (1999).CAS 
    PubMed 
    Article 

    Google Scholar 
    29.Pexton, J. J. & Mayhew, P. J. Immobility: The key to family harmony?. Trends. Ecol. Evol. 16, 7–9 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    30.Hamilton, W. D. Extraordinary sex ratios. Science 156, 477–488 (1967).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    31.Mayhew, P. J. & Hardy, I. C. Nonsiblicidal behavior and the evolution of clutch size in bethylid wasps. Am. Nat. 151, 409–424 (1998).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    32.Zaviezo, T. & Mills, N. Factors influencing the evolution of clutch size in a gregarious insect parasitoid. J. Anim. Ecol. 69, 1047–1057 (2000).Article 

    Google Scholar 
    33.Koppik, M., Tiel, A. & Hofmeister, T. S. Adaptive decision making or diferential mortality: What causes ofspring emergence in a gregarious parasitoid?. Entomol. Exp. Appl. 150, 208–216 (2014).Article 

    Google Scholar 
    34.Visser, M. E., Van Alphen, J. J. & Hemerik, L. Adaptive superparasitism and patch time allocation in solitary parasitoids: An ESS model. J. Anim. Ecol. 61, 93–101 (1992).Article 

    Google Scholar 
    35.Waage, J. K. & Ming, N. S. The reproductive strategy of a parasitic wasp: I. optimal progeny and sex allocation in Trichogramma evanescens. J. An. Ecol. 53, 401–415 (1984).Article 

    Google Scholar 
    36.Harvey, J. A., Poelman, E. H. & Tanaka, T. Intrinsic inter-and intraspecific competition in parasitoid wasps. Ann. Rev. Entomol. 58, 333–351 (2013).CAS 
    Article 

    Google Scholar 
    37.Harvey, J. A., Bezemer, T. M., Gols, R., Nakamatsu, Y. & Tanaka, T. Comparing the physiological effects and function of larval feeding in closely-related endoparasitoids (Braconidae: Microgastrinae). Physiol. Entomol. 33, 217–225 (2008).Article 

    Google Scholar 
    38.Cloutier, C., Duperron, J., Tertuliano, M. & McNeil, J. N. Host instar, body size and fitness in the koinobiotic parasitoid Aphidius nigripes. Entomol. Exp. Appl. 97, 29–40 (2000).Article 

    Google Scholar 
    39.Bai, B., Luck, R. F., Forster, L., Stephens, B. & Janssen, J. M. The effect of host size on quality attributes of the egg parasitoid Trichogramma pretiosum. Entomol. Exp. Appl. 64, 37–48 (1992).Article 

    Google Scholar 
    40.Kazmer, D. J. & Luck, R. F. Field tests of the size-fitness hypothesis in the egg parasitoid Trichogramma Pretiosum. Ecology 76, 412–425 (1995).Article 

    Google Scholar 
    41.Samková, A., Hadrava, J., Skuhrovec, J. & Janšta, P. Reproductive strategy as a major factor determining female body size and fertility of a gregarious parasitoid. J. Appl. Entomol. 143, 441–450 (2019).Article 

    Google Scholar 
    42.Wei, K., Tang, Y. L., Wang, X. Y., Cao, L. M. & Yang, Z. Q. The developmental strategies and related profitability of an idiobiont ectoparasitoid Sclerodermus pupariae vary with host size. Ecol. Entomol. 39, 101–108 (2014).Article 

    Google Scholar 
    43.May, R. M., Hassell, M. P., Anderson, M. R. & Tonkyn, D. V. Density dependence in host-parasitoid models. J. Anim. Ecol. 50, 855–865 (1981).MathSciNet 
    Article 

    Google Scholar 
    44.Hoddle, M. S., Van Driesche, R. G., Elkinton, J. S. & Sanderson, J. P. Discovery and utilization of Bemisia argentifolii patches by Eretmocerus eremicus and Encarsia formosa (Beltsville strain) in greenhouses. Entomol. Exp. Appl. 87, 15–28 (1998).Article 

    Google Scholar 
    45.Samková, A., Raska, J., Hadrava, J. & Skuhrovec, J. An intergenerational approach for prediction of parasitoid population dynamics. BioRxiv. https://doi.org/10.1101/2021.02.22.432341 (2021).Article 

    Google Scholar 
    46.Anderson, R. C. & Paschke, J. D. The biology and ecology of Anaphes flavipes (Hymenoptera: Mymaridae), an exotic egg parasite of the cereal leaf beetle. Ann. Entomol. Soc. Am. 61, 1–5 (1968).Article 

    Google Scholar 
    47.Klomp, H. & Teerink, B. J. The significance of oviposition rates in the egg parasite Trichogramma embryophagum Htg. Arch. Neerl. Zool. 17, 350–375 (1967).Article 

    Google Scholar 
    48.Waage, J. K. & Lane, J. A. The reproductive strategy of a parasitic wasp: II. Sex allocation and local mate competition in Trichogramma evanescens. J. Anim. Ecol. 53, 417–426 (1984).Article 

    Google Scholar 
    49.Dysart, R. J., Maltby, H. L. & Brunson, M. H. Larval parasites of Oulema melanopus in Europe and their colonization in the United States. Entomophaga 18, 133–167 (1973).Article 

    Google Scholar 
    50.Skuhrovec, J. et al. Insecticidal activity of two formulations of essential oils against the cereal leaf beetle. Acta Agr. Scand. 68, 489–495 (2018).CAS 

    Google Scholar 
    51.Jervis, M. A., Ellers, J. & Harvey, J. A. Resource acquisition, allocation, and utilization in parasitoid reproductive strategies. Annu. Rev. Entomol. 53, 361–385 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    52.Vinson, S. B. & Iwantsch, G. F. Host suitability for insect parasitoids. Ann. Rev. Entomol. 25, 397–419 (1980).Article 

    Google Scholar 
    53.Mackauer, M., Sequeira, R. & Otto, M. Growth and development in parasitoid wasps adaptation to variable host resources. In Vertical Food Web Interactions 191–203 (Springer, 1997).Chapter 

    Google Scholar 
    54.Ode, P. J. Plant toxins and parasitoid trophic ecology. Curr. Opin. Insect sci. 32, 118–123 (2019).PubMed 
    Article 

    Google Scholar 
    55.Cronin, J. T. & Abrahamson, W. G. Do parasitoids diversify in response to host-plant shifts by herbivorous insects?. Ecol. Entomol. 26, 347–355 (2001).Article 

    Google Scholar 
    56.Sarfraz, M., Dosdall, L. M. & Keddie, B. A. Host plant nutritional quality affects the performance of the parasitoid Diadegma insulare. Biol. Control. 51, 34–41 (2009).CAS 
    Article 

    Google Scholar 
    57.Harvey, J. A. Factors affecting the evolution of development strategies in parasitoid wasps: The importance of functional constraints and incorporating complexity. Entomol. Exp. Appl. 117, 1–13 (2005).Article 

    Google Scholar 
    58.Cortesero, A. M. & Monge, J. P. Influence of pre-emergence experience on response to host and host plant odours in the larval parasitoid Eupelmus vuilleti. Entomol. Exp. Appl. 72, 281–288 (1994).Article 

    Google Scholar 
    59.Gandolfi, M., Mattiacci, L. & Dorn, S. Preimaginal learning determines adult response to chemical stimuli in a parasitic wasp. Proc. Roy. Soc. Lon. Series. B-Biol. Scien. 270, 2623–2629 (2003).Article 

    Google Scholar 
    60.Kester, K. M. & Barbosa, P. Postemergence learning in the insect parasitoid, Cotesia congregata (Say) (Hymenoptera: Braconidae). J. Insect Behav. 4, 727–742 (1991).Article 

    Google Scholar 
    61.Vet, L. E. & Groenewold, A. W. Semiochemicals and learning in parasitoids. J. Chem. Ecol. 16, 3119–3135 (1990).CAS 
    PubMed 
    Article 

    Google Scholar 
    62.Samková, A., Hadrava, J., Skuhrovec, J. & Janšta, P. Effect of adult feeding and timing of host exposure on the fertility and longevity of the parasitoid Anaphes flavipes. Entomol. Exp. Appl. 167, 932–938 (2019).Article 

    Google Scholar 
    63.Jervis, M. A., Heimpel, G. E., Ferns, P. N., Harvey, J. A. & Kidd, N. A. Life-history strategies in parasitoid wasps: A comparative analysis of ‘ovigeny’. J. Anim. Ecol. 70, 442–458 (2001).Article 

    Google Scholar 
    64.Bjorksten, T. A. & Hoffmann, A. A. Persistence of experience effects in the parasitoid Trichogramma nr. brassicae. Ecol. Entomol. 23, 110–117 (1998).Article 

    Google Scholar 
    65.Lentz, A. J. & Kester, K. M. Postemergence experience affects sex ratio allocation in a gregarious insect parasitoid. J. Insect. Behav. 21, 34–45 (2008).Article 

    Google Scholar 
    66.Nishida, R. Sequestration of defensive substances from plants by Lepidoptera. Annu. Rev. Entomol. 47, 57–92 (2002).CAS 
    PubMed 
    Article 

    Google Scholar 
    67.Zvereva, E. L. & Rank, N. E. Fly parasitoid Megaselia opacicornis uses defensive secretions of the leaf beetle Chrysomela lapponica to locate its host. Oecologia 140, 516–522 (2004).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    68.Roy, H. E., Handley, L. J. L., Schönrogge, K., Poland, R. L. & Purse, B. V. Can the enemy release hypothesis explain the success of invasive alien predators and parasitoids?. Biocontrol 56, 451–468 (2011).Article 

    Google Scholar 
    69.Snyder, W. E. & Ives, A. R. Interactions between specialist and generalist natural enemies: Parasitoids, predators, and pea aphid biocontrol. Ecology 84, 91–107 (2003).Article 

    Google Scholar 
    70.Polis, G. A., Myers, C. A. & Holt, R. D. The ecology and evolution of intraguild predation: Potential competitors that eat each other. Annu. Rev. Ecol. Syst. 20, 297–330 (1989).Article 

    Google Scholar 
    71.Nakashima, Y. & Senoo, N. Avoidance of ladybird trails by an aphid parasitoid Aphidius ervi: active period and efects of prior oviposition experience. Entomol. Exp. Appl. 109, 163–166 (2003).Article 

    Google Scholar 
    72.Samková, A., Raška, J., Hadrava, J., Skuhrovec, J. & Janšta, P. Female manipulation of offspring sex ratio in the gregarious parasitoid Anaphes flavipes from a new two-generation approach. BioRxiv https://doi.org/10.1101/2021.02.22.432331 (2021).Article 

    Google Scholar 
    73.Visser, M. E. The importance of being large: the relationship between size and fitness in females of the parasitoid Aphaereta minuta (Hymenoptera: Braconidae). J. Anim. Ecol. 63, 963–978 (1994).Article 

    Google Scholar 
    74.Banks, M. & Thomson, D. J. Lifetime mating success in the damselfly Coenagrion puella. Anim. Behav. 33, 1175–1183 (1985).Article 

    Google Scholar 
    75.Ellers, J. & Jervis, M. Body size and the timing of egg production in parasitoid wasps. Oikos 102, 164–172 (2003).Article 

    Google Scholar 
    76.Anderson, R. C. & Paschke, J. D. Additional Observations on the Biology of Anaphes flavipes (Hymenoptera: Mymaridae), with Special Reference to the Efects of Temperature and Superparasitism on Development. Ann. Entomol. Soc. Am. 62, 1316–1321 (1969).Article 

    Google Scholar 
    77.Bezděk, J. & Baselga, A. Revision of western Palaearctic species of the Oulema melanopus group, with description of two new species from Europe (Coleoptera: Chrysomelidae: Criocerinae). Acta. Ent. Mus. Nat. Pra. 55, 273–304 (2015).
    Google Scholar 
    78.R. Core Team R. A language and environment for statistical computing. R Foundation for Statistical Computing (R Core Team, 2020).
    Google Scholar 
    79.Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting Linear Mixed-Effects Models Using lme4. J. Stat. Softw 67, 1–48. (2015) URL: https://CRAN.R-project.org/package=Hmisc.80.Harrell, F. E. Jr, Dupont, C., et mult. al. (2020) Hmisc: Harrell Miscellaneous. R package version 4.4–2. URL: https://CRAN.R-project.org/package=Hmisc.81.Signorell et mult. al. (2021). DescTools: Tools for descriptive statistics. R package version 0.99.40. URL: https://cran.r-project.org/package=DescTools. More

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    AusTraits, a curated plant trait database for the Australian flora

    1.Zanne, A. E. et al. Three keys to the radiation of angiosperms into freezing environments. Nature 506, 89 (2014).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    2.Cornwell, W. K. et al. Functional distinctiveness of major plant lineages. J. Ecol. 102, 345–356 (2014).Article 

    Google Scholar 
    3.Díaz, S. et al. The global spectrum of plant form and function. Nature 529, 167 (2016).ADS 
    PubMed 
    Article 
    CAS 

    Google Scholar 
    4.Kunstler, G. et al. Plant functional traits have globally consistent effects on competition. Nature 529, 204 (2016).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    5.Chapin, F. S. III, Autumn, K. & Pugnaire, F. Evolution of suites of traits in response to environmental stress. Am. Nat. 142, S78–S92 (1993).Article 

    Google Scholar 
    6.Adler, P. B. et al. Functional traits explain variation in plant life history strategies. Proc. Natl. Acad. Sci. USA 111, 740–745 (2014).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    7.Diaz, S., Cabido, M. & Casanoves, F. Plant functional traits and environmental filters at a regional scale. J. Veg. Sci. 9, 113–122 (1998).Article 

    Google Scholar 
    8.Violle, C. et al. Let the concept of trait be functional! Oikos 116, 882–892 (2007).Article 

    Google Scholar 
    9.Westoby, M. A leaf-height-seed (LHS) plant ecol. Strategy scheme. Plant Soil 199, 213–227 (1998).CAS 
    Article 

    Google Scholar 
    10.Funk, J. L. et al. Revisiting the holy grail: Using plant functional traits to understand ecological processes. Biol. Rev. 92, 1156–1173 (2017).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    11.Kattge, J. et al. TRY a global database of plant traits. Glob. Chang. Biol. 17, 2905–2935 (2011).ADS 
    PubMed Central 
    Article 

    Google Scholar 
    12.Kattge, J. et al. TRY plant trait database enhanced coverage and open access. Glob. Chang. Biol. 26, 119–188 (2020).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    13.CHAH. Australian Plant Census, Centre of Australian National Biodiversity Research. https://id.biodiversity.org.au/tree/51354547 (2020).14.Kissling, W. D. et al. Towards global data products of Essential Biodiversity Variables on species traits. Nat. Ecol. Evol. 2, 1531–1540 (2018).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    15.Gallagher, R. V. et al. Open Science principles for accelerating trait-based science across the Tree of Life. Nat. Ecol. Evol. 4, 294–303 (2020).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    16.Chapman, A. D. et al. Numbers of living species in Australia and the world. (Australian Government, 2009).17.Hopper, S. D. & Gioia, P. The Southwest Australian Floristic Region: Evolution and conservation of a global hot spot of biodiversity. Annual Review of Ecology, Evolution, and Systematics 35, 623–650 (2004).Article 

    Google Scholar 
    18.Madin, J. et al. An ontology for describing and synthesizing ecological observation data. Ecol. Inform. 2, 279–296 (2007).Article 

    Google Scholar 
    19.Garnier, E. et al. Towards a thesaurus of plant characteristics: An ecological contribution. J. Ecol. 105, 298–309 (2017).Article 

    Google Scholar 
    20.Adams, M. A. M, P. & Attiwill. Role of Acacia spp. in nutrient balance and cycling in regenerating Eucalyptus regnans F. Muell. forests. I. Temporal changes in biomass and nutrient content. Aust. J. Bot. 32, 205–215 (1984).CAS 

    Google Scholar 
    21.Ahrens, C. W. et al. Plant functional traits differ in adaptability and are predicted to be differentially affected by climate change. Ecol. Evo. 10, 232–248 (2019).Article 

    Google Scholar 
    22.Australian National Botanic Gardens. The National Seed Bank. http://www.anbg.gov.au/gardens/living/seedbank/ (2018).23.Angevin, T. Species richness and functional trait diversity response to land use in a temperate eucalypt woodland community. (La Trobe University, 2011).24.Apgaua, D. M. G. et al. Functional traits and water transport strategies in lowland tropical rainforest trees. PLoS One 10, e0130799 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    25.Apgaua, D. M. G. et al. Plant functional groups within a tropical forest exhibit different wood functional anatomy. Funct. Ecol. 31, 582–591 (2017).Article 

    Google Scholar 
    26.Ashton, D. H. Studies of litter in Eucalyptus regnans forests. Aust. J. Bot. 23, 413–433 (1975).CAS 
    Article 

    Google Scholar 
    27.Ashton, D. H. Phosphorus in forest ecosystems at Beenak, Victoria. The J. Ecol. 64, 171–186 (1976).CAS 

    Google Scholar 
    28.Attiwill, P. M. Nutrient cycling in a Eucalyptus obliqua (L’Herit.) forest IV: Nutrient uptake and nutrient return. Aust. J. Bot. 28, 199–222 (1980).CAS 
    Article 

    Google Scholar 
    29.Barlow, B. A., Clifford, H. T., George, A. S. & McCusker, A. K. A. Flora of Australia. http://www.environment.gov.au/biodiversity/abrs/online-resources/flora/main/ (1981).30.Bean, A. R. A revision of Baeckea (Myrtaceae) in eastern Australia, Malesia and south-east Asia. Telopea 7, 245–268 (1997).Article 

    Google Scholar 
    31.Bell, L.C. Nutrient requirements for the establishment of native flora at Weipa. (Comalco Aluminium Ltd., 1985).32.Bennett, L. T. & Attiwill, P. M. The nutritional status of healthy and declining stands of Banksia integrifolia on the Yanakie Isthmus, Victoria. Aust. J. Bot. 45, 15–30 (1997).Article 

    Google Scholar 
    33.Bevege, D. I. Biomass and nutrient distribution in indigenous forest ecosystems. vol. 6 20 (Queensland Department of Forestry, 1978).34.Birk, E. M. & Turner, J. Response of flooded gum (E. grandis) to intensive cultural treatments: biomass and nutrient content of eucalypt plantations and native forests. For. Ecol. Manage. 47, 1–28 (1992).Article 

    Google Scholar 
    35.Blackman, C. J., Brodribb, T. J. & Jordan, G. J. Leaf hydraulic vulnerability is related to conduit dimensions and drought resistance across a diverse range of woody angiosperms. New Phytol. 188, 1113–1123 (2010).PubMed 
    Article 

    Google Scholar 
    36.Blackman, C. J. et al. Leaf hydraulic vulnerability to drought is linked to site water availability across a broad range of species and climates. Ann. Bot. 114, 435–440 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    37.Blackman, C. J. et al. The links between leaf hydraulic vulnerability to drought and key aspects of leaf venation and xylem anatomy among 26 Australian woody angiosperms from contrasting climates. Ann. Bot. 122, 59–67 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    38.Bloomfield, K. J. et al. A continental-scale assessment of variability in leaf traits: Within species, across sites and between seasons. Funct. Ecol. 32, 1492–1506 (2018).Article 

    Google Scholar 
    39.Bolza, E. Properties and uses of 175 timber species from Papua New Guinea and West Irian. (Victoria (Australia) CSIRO, Div. of Building Research, 1975).40.Bragg, J. G. & Westoby, M. Leaf size and foraging for light in a sclerophyll woodland. Funct. Ecol. 16, 633–639 (2002).Article 

    Google Scholar 
    41.Brisbane Rainforest Action and Information Network. Trait measurements for Australian rainforest species. http://www.brisrain.org.au/ (2016).42.Briggs, A. L. & Morgan, J. W. Seed characteristics and soil surface patch type interact to affect germination of semi-arid woodland species. Plant Ecol. 212, 91–103 (2010).Article 

    Google Scholar 
    43.Brock, J. & Dunlop, A. Native plants of northern Australia. (Reed New Holland, 1993).44.Brodribb, T. J. & Cochard, H. Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiol. 149, 575–584 (2009).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    45.Buckton, G. et al. Functional traits of lianas in an Australian lowland rainforest align with post-disturbance rather than dry season advantage. Austral Ecol. 44, 983–994 (2019).Article 

    Google Scholar 
    46.Burgess, S. S. O. & Dawson, T. E. Predicting the limits to tree height using statistical regressions of leaf traits. New Phytol. 174, 626–636 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    47.Burrows, G. E. Comparative anatomy of the photosynthetic organs of 39 xeromorphic species from subhumid New South Wales, Australia. Int. J. Plant Sci. 162, 411–430 (2001).Article 

    Google Scholar 
    48.Butler, D. W., Gleason, S. M., Davidson, I., Onoda, Y. & Westoby, M. Safety and streamlining of woody shoots in wind: an empirical study across 39 species in tropical Australia. New Phytol. 193, 137–149 (2011).PubMed 
    Article 

    Google Scholar 
    49.CAB International. Forestry Compendium. http://www.cabi.org/fc/ (2009).50.Caldwell, E., Read, J. & Sanson, G. D. Which leaf mechanical traits correlate with insect herbivory among feeding guilds? Ann. Bot. 117, 349–361 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    51.Canham, C. A., Froend, R. H. & Stock, W. D. Water stress vulnerability of four Banksia species in contrasting ecohydrological habitats on the Gnangara Mound. Western Australia. Plant Cell Envrion. 32, 64–72 (2009).Article 

    Google Scholar 
    52.Carpenter, R. J. Cuticular morphology and aspects of the ecology and fossil history of North Queensland rainforest Proteaceae. Bot. J. Linn. Soc. 116, 249–303 (1994).Article 

    Google Scholar 
    53.Carpenter, R. J., Hill, R. S. & Jordan, G. J. Leaf Cuticular Morphology Links Platanaceae and Proteaceae. Int. J. Plant Sci. 166, 843–855 (2005).Article 

    Google Scholar 
    54.Catford, J. A., Downes, B. J., Gippel, C. J. & Vesk, P. A. Flow regulation reduces native plant cover and facilitates exotic invasion in riparian wetlands. J. Appl. Ecol. 48, 432–442 (2011).Article 

    Google Scholar 
    55.Catford, J. A., Morris, W. K., Vesk, P. A., Gippel, C. J. & Downes, B. J. Species and environmental characteristics point to flow regulation and drought as drivers of riparian plant invasion. Divers. Distrib. 20, 1084–1096 (2014).Article 

    Google Scholar 
    56.Cernusak, L. A., Hutley, L. B., Beringer, J. & Tapper, N. J. Stem and leaf gas exchange and their responses to fire in a north Australian tropical savanna. Plant Cell Envrion. 29, 632–646 (2006).Article 

    Google Scholar 
    57.Cernusak, L. A., Hutley, L. B., Beringer, J., Holtum, J. A. M. & Turner, B. L. Photosynthetic physiology of eucalypts along a sub-continental rainfall gradient in northern Australia. Agric. For. Meteorol. 151, 1462–1470 (2011).ADS 
    Article 

    Google Scholar 
    58.Chandler, G. T., Crisp, M. D., Cayzer, L. W. & Bayer, R. J. Monograph of Gastrolobium (Fabaceae: Mirbelieae). Aust. Syst. Bot. 15, 619–739 (2002).Article 

    Google Scholar 
    59.Chave, J. et al. Towards a worldwide wood economics spectrum. Ecol. Lett. 12, 351–366 (2009).PubMed 
    Article 

    Google Scholar 
    60.Cheal, D. Growth stages and tolerable fire intervals for Victoria’s native vegetation data sets. (Victorian Government Department of Sustainability; Environment Melbourne, 2010).61.Cheesman, A. W., Duff, H., Hill, K., Cernusak, L. A. & McInerney, F. A. Isotopic and morphologic proxies for reconstructing light environment and leaf function of fossil leaves: A modern calibration in the Daintree Rainforest, Australia. Am. J. Bot. 107, 1165–1176 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    62.Chen et al. Plants show more flesh in the tropics: Variation in fruit type along latitudinal and climatic gradients. Ecography 40, 531–538 (2017).Article 

    Google Scholar 
    63.Chinnock, R. J. Eremophila and allied genera: A monograph of the plant family Myoporaceae. (Rosenberg, 2007).64.Choat, B., Ball, M. C., Luly, J. G. & Holtum, J. A. M. Hydraulic architecture of deciduous and evergreen dry rainforest tree species from north-eastern Australia. Trees 19, 305–311 (2005).Article 

    Google Scholar 
    65.Choat, B., Ball, M. C., Luly, J. G., Donnelly, C. F. & Holtum, J. A. M. Seasonal patterns of leaf gas exchange and water relations in dry rain forest trees of contrasting leaf phenology. Tree Physiol. 26, 657–664 (2006).PubMed 
    Article 

    Google Scholar 
    66.Choat, B. et al. Global convergence in the vulnerability of forests to drought. Nature 491, 752–755 (2012).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    67.Chudnoff, M. Tropical timbers of the world. 472 (US Department of Agriculture, Forest Service, 1984).68.The French agricultural research and international cooperation organization (CIRAD). Wood density data. http://www.cirad.fr/ (2009).69.Clarke, P. J. et al. A synthesis of postfire recovery traits of woody plants in Australian ecosystems. Sci. Total Environ. 534, 31–42 (2015).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    70.Cooper, W. & Cooper, W. T. Fruits of the Australian tropical rainforest. (Nokomis Editions, 2004).71.Cooper, W. & Cooper, W. T. Australian rainforest fruits. 272 (CSIRO Publishing, 2013).72.Cornwell, W. K. Causes and consequences of functional trait diversity: plant community assembly and leaf decomposition. (Stanford University, California, 2006).73.Centre for Plant Biodiversity Research. EUCLID 2.0: Eucalypts of Australia. http://apps.lucidcentral.org/euclid/text/intro/index.html (2002).74.Craven, L. A., A taxonomic revision of Calytrix Labill. (Myrtaceae). Brunonia 10, 1–138 (1987).Article 

    Google Scholar 
    75.Craven, L. A., Lepschi, B. J. & Cowley, K. J. Melaleuca (Myrtaceae) of Western Australia: Five new species, three new combinations, one new name and a new state record. Nuytsia 20, 27–36 (2010).
    Google Scholar 
    76.Crisp, M. D., Cayzer, L., Chandler, G. T. & Cook, L. G. A monograph of Daviesia (Mirbelieae, Faboideae, Fabaceae). Phytotaxa 300, 1–308 (2017).Article 

    Google Scholar 
    77.Cromer, R. N., Raupach, M., Clarke, A. R. P. & Cameron, J. N. Eucalypt plantations in Australia – the potential for intensive production and utilization. Appita J. 29, 165–173 (1975).
    Google Scholar 
    78.Cross, E. The characteristics of natives and invaders: A trait-based investigation into the theory of limiting similarity. (La Trobe University, 2009).79.Crous, K. Y. et al. Photosynthesis of temperate Eucalyptus globulus trees outside their native range has limited adjustment to elevated CO2 and climate warming. Glob. Chang. Biol. 19, 3790–3807 (2013).ADS 
    PubMed 
    Article 

    Google Scholar 
    80.Crous, K. Y., Wujeska-Klause, A., Jiang, M., Medlyn, B. E. & Ellsworth, D. S. Nitrogen and phosphorus retranslocation of leaves and stemwood in a mature Eucalyptus forest exposed to 5 years of elevated CO2. Front. Plant. Sci. 10, art664 (2019).Article 

    Google Scholar 
    81.Cunningham, S. A., Summerhayes, B. & Westoby, M. Evolutionary divergences in leaf structure and chemistry, comparing rainfall and soil nutrient gradients. Ecol. Monogr. 69, 569–588 (1999).Article 

    Google Scholar 
    82.Curran, T. J., Clarke, P. J. & Warwick, N. W. M. Water relations of woody plants on contrasting soils during drought: does edaphic compensation account for dry rainforest distribution? Aust. J. Bot. 57, 629–639 (2009).Article 

    Google Scholar 
    83.Curtis, E. M., Leigh, A. & Rayburg, S. Relationships among leaf traits of Australian arid zone plants: alternative modes of thermal protection. Aust. J. Bot. 60, 471–483 (2012).Article 

    Google Scholar 
    84.Denton, M. D., Veneklaas, E. J., Freimoser, F. M. & Lambers, H. Banksia species (Proteaceae) from severely phosphorus-impoverished soils exhibit extreme efficiency in the use and re-mobilization of phosphorus. Plant Cell Envrion. 30, 1557–1565 (2007).CAS 
    Article 

    Google Scholar 
    85.Desch, H. E. & Dinwoodie, J. M. Timber structure, properties, conversion and use. (Palgrave Macmillan, 1996).86.de Tombeur, F. et al. A shift from phenol to silica-based leaf defenses during long-term soil and ecosystem development. Ecol. Lett. 24, 984–995 (2021).PubMed 
    Article 

    Google Scholar 
    87.Dong, N. et al. Leaf nitrogen from first principles: field evidence for adaptive variation with climate. Biogeosciences 14, 481–495 (2017).ADS 
    CAS 
    Article 

    Google Scholar 
    88.Dong, N. et al. Components of leaf-trait variation along environmental gradients. New Phytol. 228, 82–94 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    89.Du, P., Arndt, S. K. & Farrell, C. Relationships between plant drought response, traits, and climate of origin for green roof plant selection. Ecol. Appl. 28, 1752–1761 (2018).PubMed 
    Article 

    Google Scholar 
    90.Du, P., Arndt, S. K. & Farrell, C. Can the turgor loss point be used to assess drought response to select plants for green roofs in hot and dry climates? Plant Soil 441, 399–408 (2019).CAS 
    Article 

    Google Scholar 
    91.Duan, H. et al. Drought responses of two gymnosperm species with contrasting stomatal regulation strategies under elevated [CO2] and temperature. Tree Physiol. 35, 756–770 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    92.Duncan, R. P. et al. Plant traits and extinction in urban areas: a meta-analysis of 11 cities. Glob. Ecol. Biog. 20, 509–519 (2011).Article 

    Google Scholar 
    93.Dwyer, J. M. & Laughlin, D. C. Constraints on trait combinations explain climatic drivers of biodiversity: The importance of trait covariance in community assembly. Ecol. Lett. 20, 872–882 (2017).PubMed 
    Article 

    Google Scholar 
    94.Dwyer, J. M. & Mason, R. Plant community responses to thinning in densely regenerating Acacia harpophylla forest. Restor. Ecol. 26, 97–105 (2018).Article 

    Google Scholar 
    95.Eamus, D. & Prichard, H. A cost-benefit analysis of leaves of four Australian savanna species. Tree Physiol. 18, 537–545 (1998).PubMed 
    Article 

    Google Scholar 
    96.Eamus, D., Myers, B., Duff, G. & Williams, D. Seasonal changes in photosynthesis of eight savanna tree species. Tree Physiol. 19, 665–671 (1999).PubMed 
    Article 

    Google Scholar 
    97.Myers, B., E., D. & Duff, G. A cost-benefit analysis of leaves of eight Australian savanna tree species of differing life-span. Photosynthetica 36, 575–586 (1999).Article 

    Google Scholar 
    98.Edwards, C., Read, J. & Sanson, G. D. Characterising sclerophylly: some mechanical properties of leaves from heath and forest. Oecologia 123, 158–167 (2000).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    99.Edwards, C., Sanson, G. D., Aranwela, N. & Read, J. Relationships between sclerophylly, leaf biomechanical properties and leaf anatomy in some Australian heath and forest species. Plant Biosyst. 134, 261–277 (2000).Article 

    Google Scholar 
    100.Schöenenberger, J. et al. Phylogenetic analysis of fossil flowers using an angiosperm-wide data set: proof-of-concept and challenges ahead. Am. J. Bot. 107, 1433–1448 (2020).Article 

    Google Scholar 
    101.Esperon-Rodriguez, M. et al. Functional adaptations and trait plasticity of urban trees along a climatic gradient. Urban For. Urban Green. 54, art126771 (2020).Article 

    Google Scholar 
    102.Everingham, S. E., Offord, C. A., Sabot, M. E. B. & Moles, A. T. Time travelling seeds reveal that plant regeneration and growth traits are responding to climate change. Ecology 102, e03272 (2020).
    Google Scholar 
    103.Falster, D. S. & Westoby, M. Leaf size and angle vary widely across species: what consequences for light interception? New Phytol. 158, 509–525 (2003).Article 

    Google Scholar 
    104.Falster, D. S. & Westoby, M. Alternative height strategies among 45 dicot rain forest species from tropical Queensland, Australia. J. Ecol. 93, 521–535 (2005).Article 

    Google Scholar 
    105.Falster, D. S. & Westoby, M. Tradeoffs between height growth rate, stem persistence and maximum height among plant species in a post-fire succession. Oikos 111, 57–66 (2005).Article 

    Google Scholar 
    106.Farrell, C., Mitchell, R. E., Szota, C., Rayner, J. P. & Williams, N. S. G. Green roofs for hot and dry climates: Interacting effects of plant water use, succulence and substrate. Ecol. Eng. 49, 270–276 (2012).Article 

    Google Scholar 
    107.Farrell, C., Szota, C., Williams, N. S. G. & Arndt, S. K. High water users can be drought tolerant: using physiological traits for green roof plant selection. Plant Soil 372, 177–193 (2013).CAS 
    Article 

    Google Scholar 
    108.Farrell, C., Szota, C. & Arndt, S. K. Does the turgor loss point characterize drought response in dryland plants? Plant Cell Envrion. 40, 1500–1511 (2017).CAS 
    Article 

    Google Scholar 
    109.Feller, M. C. Biomass and nutrient distribution in two eucalypt forest ecosystems. Austral Ecol. 5, 309–333 (1980).Article 

    Google Scholar 
    110.Firn, J. et al. Leaf nutrients, not specific leaf area, are consistent indicators of elevated nutrient inputs. Nature Ecol. Evo. 3, 400–406 (2019).Article 

    Google Scholar 
    111.Flynn, J. H. & Holder, C. D. A guide to useful woods of the world. (Forest Products Society, 2001).112.Fonseca, C. R., Overton, J. M. C., Collins, B. & Westoby, M. Shifts in trait-combinations along rainfall and phosphorus gradients. J. Ecol. 88, 964–977 (2000).Article 

    Google Scholar 
    113.McDonald, P. G., Fonseca, C. R., Overton, J. M. C. & Westoby, M. Leaf-size divergence along rainfall and soil-nutrient gradients: is the method of size reduction common among clades? Funct. Ecol. 17, 50–57 (2003).Article 

    Google Scholar 
    114.Forster, P. I. A taxonomic revision of Alyxia (Apocynaceae) in Australia. Aust. Syst. Bot. 5, 547–580 (1992).Article 

    Google Scholar 
    115.Forster, P. I. New names and combinations in Marsdenia (Asclepiadaceae: Marsdenieae) from Asia and Malesia (excluding Papusia). Aust. Syst. Bot. 8, 691–701 (1995).Article 

    Google Scholar 
    116.French, B. J., Prior, L. D., Williamson, G. J. & Bowman, D. M. J. S. Cause and effects of a megafire in sedge-heathland in the Tasmanian temperate wilderness. Aust. J. Bot. 64, 513–525 (2016).Article 

    Google Scholar 
    117.Froend, R. H. & Drake, P. L. Defining phreatophyte response to reduced water availability: preliminary investigations on the use of xylem cavitation vulnerability in Banksia woodland species. Aust. J. Bot. 54, 173–179 (2006).Article 

    Google Scholar 
    118.Funk, J. L., Standish, R. J., Stock, W. D. & Valladares, F. Plant functional traits of dominant native and invasive species in mediterranean-climate ecosystems. Ecology 97, 75–83 (2016).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    119.Gallagher, R. V. et al. Invasiveness in introduced Australian acacias: The role of species traits and genome size. Divers. Distrib. 17, 884–897 (2011).Article 

    Google Scholar 
    120.Gallagher, R. V. & Leishman, M. R. A global analysis of trait variation and evolution in climbing plants. J. Biogeogr. 39, 1757–1771 (2012).Article 

    Google Scholar 
    121.Gardiner, R., Shoo, L. P. & Dwyer John. M. Look to seedling heights, rather than functional traits, to explain survival during extreme heat stress in the early stages of subtropical rainforest restoration. J. Appl. Ecol. 56, 2687–2697 (2019).Article 

    Google Scholar 
    122.Geange, S. R. et al. Phenotypic plasticity and water availability: responses of alpine herb species along an elevation gradient. Clim. Change Responses 4, 1–12 (2017).Article 

    Google Scholar 
    123.Geange, S. R., Holloway-Phillips, M.-M., Briceno, V. F. & Nicotra, A. B. Aciphylla glacialis mortality, growth and frost resistance: a field warming experiment. Aust. J. Bot. 67, 599–609 (2020).Article 

    Google Scholar 
    124.Ghannoum, O. et al. Exposure to preindustrial, current and future atmospheric CO2 and temperature differentially affects growth and photosynthesis in Eucalyptus. Glob. Chang. Biol. 16, 303–319 (2010).ADS 
    Article 

    Google Scholar 
    125.Gleason, S. M., Butler, D. W., Zieminska, K., Waryszak, P. & Westoby, M. Stem xylem conductivity is key to plant water balance across Australian angiosperm species. Funct. Ecol. 26, 343–352 (2012).Article 

    Google Scholar 
    126.Gleason, S. M., Butler, D. W. & Waryszak, P. Shifts in leaf and stem hydraulic traits across aridity gradients in eastern Australia. Int. J. Plant Sci. 174, 1292–1301 (2013).Article 

    Google Scholar 
    127.Gleason, S. M., Blackman, C. J., Cook, A. M., Laws, C. A. & Westoby, M. Whole-plant capacitance, embolism resistance and slow transpiration rates all contribute to longer desiccation times in woody angiosperms from arid and wet habitats. Tree Physiol. 34, 275–284 (2014).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    128.Gleason, S. M. et al. Vessel scaling in evergreen angiosperm leaves conforms with Murray’s law and area-filling assumptions: implications for plant size, leaf size and cold tolerance. New Phytol. 218, 1360–1370 (2018).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    129.Goble-Garratt, E., Bell, D. & Loneragan, W. Floristic and leaf structure patterns along a shallow elevational gradient. Aust. J. Bot. 29, 329–347 (1981).Article 

    Google Scholar 
    130.Gosper, C. R. Fruit characteristics of invasive bitou bush, Chrysanthemoides monilifera (Asteraceae), and a comparison with co-occurring native plant species. Aust. J. Bot. 52, 223–230 (2004).Article 

    Google Scholar 
    131.Gosper, C. R., Yates, C. J. & Prober, S. M. Changes in plant species and functional composition with time since fire in two mediterranean climate plant communities. J. Veg. Sci. 23, 1071–1081 (2012).Article 

    Google Scholar 
    132.Gosper, C. R., Prober, S. M. & Yates, C. J. Estimating fire interval bounds using vital attributes: implications of uncertainty and among-population variability. Ecol. Appl. 23, 924–935 (2013).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    133.Gosper, C. R., Yates, C. J. & Prober, S. M. Floristic diversity in fire-sensitive eucalypt woodlands shows a “U”-shaped relationship with time since fire. J. Appl. Ecol. 50, 1187–1196 (2013).Article 

    Google Scholar 
    134.Gosper, C. R. et al. A conceptual model of vegetation dynamics for the unique obligate-seeder eucalypt woodlands of south-western Australia. Austral Ecol. 43, 681–695 (2018).Article 

    Google Scholar 
    135.Clayton, W. D., Vorontsova, M. S., Harman, K. T. & Williamson, H. GrassBase – The online world grass flora. http://www.kew.org/data/grasses-db.html (2006).136.Gray, E. F. et al. Leaf:wood allometry and functional traits together explain substantial growth rate variation in rainforest trees. AoB Plants 11, 1–11 (2019).Article 

    Google Scholar 
    137.Groom, P. K. & Lamont, B. B. Reproductive ecology of non-sprouting and re-sprouting Hakea species (Proteaceae) in southwestern Australia. In Gondwanan heritage (eds. S.D. Hopper M. Harvey, J. C. & George, A. S.) (Surrey Beatty, Chipping Norton, 1996).138.Groom, P. K. & Lamont, B. B. Fruit-seed relations in Hakea: serotinous species invest more dry matter in predispersal seed protection. Austral Ecol. 22, 352–355 (1997).Article 

    Google Scholar 
    139.Groom, P. K. & Lamont, B. B. Phosphorus accumulation in Proteaceae seeds: A synthesis. Plant Soil 334, 61–72 (2010).CAS 
    Article 

    Google Scholar 
    140.Grootemaat, S., Wright, I. J., van Bodegom, P. M., Cornelissen, J. H. C. & Cornwell, W. K. Burn or rot: leaf traits explain why flammability and decomposability are decoupled across species. Funct. Ecol. 29, 1486–1497 (2015).Article 

    Google Scholar 
    141.Grootemaat, S., Wright, I. J., van Bodegom, P. M., Cornelissen, J. H. C. & Shaw, V. Bark traits, decomposition and flammability of Australian forest trees. Aust. J. Bot. 65, 327 (2017).Article 

    Google Scholar 
    142.Grootemaat, S., Wright, I. J., van Bodegom, P. M. & Cornelissen, J. H. C. Scaling up flammability from individual leaves to fuel beds. Oikos 126, 1428–1438 (2017).Article 

    Google Scholar 
    143.Gross, C. L. The reproductive ecology of Canavalia rosea (Fabaceae) on Anak Krakatau. Indonesia. Aust. J. Bot. 41, 591–599 (1993).Article 

    Google Scholar 
    144.Gross, C. L. A comparison of the sexual systems in the trees from the Australian tropics with other tropical biomes–more monoecy but why? Am. J. Bot. 92, 907–919 (2005).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    145.Grubb, P. J. & Metcalfe, D. J. Adaptation and inertia in the Australian tropical lowland rain-forest flora: Contradictory trends in intergeneric and intrageneric comparisons of seed size in relation to light demand. Funct. Ecol. 10, 512–520 (1996).Article 

    Google Scholar 
    146.Grubb, P. J. et al. Monocot leaves are eaten less than dicot leaves in tropical lowland rain forests: Correlations with toughness and leaf presentation. Ann. Bot. 101, 1379–1389 (2008).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    147.Guilherme Pereira, C., Clode, P. L., Oliveira, R. S. & Lambers, H. Eudicots from severely phosphorus-impoverished environments preferentially allocate phosphorus to their mesophyll. New Phytol. 218, 959–973 (2018).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    148.Guilherme Pereira, C. et al. Trait convergence in photosynthetic nutrient-use efficiency along a 2-million year dune chronosequence in a global biodiversity hotspot.  J. Ecol. 107, 2006–2023 (2019).CAS 
    Article 

    Google Scholar 
    149.Hacke, U. G. et al. Water transport in vesselless Angiosperms: Conducting efficiency and cavitation safety. Int. J. Plant Sci. 168, 1113–1126 (2007).Article 

    Google Scholar 
    150.Hall, T. J. The nitrogen and phosphorus concentrations of some pasture species in the Dichanthium-Eulalia Grasslands of North-West Queensland. Rangeland J. 3, 67–73 (1981).Article 

    Google Scholar 
    151.Harrison, M. T., Edwards, E. J., Farquhar, G. D., Nicotra, A. B. & Evans, J. R. Nitrogen in cell walls of sclerophyllous leaves accounts for little of the variation in photosynthetic nitrogen-use efficiency. Plant Cell Envrion. 32, 259–270 (2009).CAS 
    Article 

    Google Scholar 
    152.Hassiotou, F., Evans, J. R., Ludwig, M. & Veneklaas, E. J. Stomatal crypts may facilitate diffusion of CO2 to adaxial mesophyll cells in thick sclerophylls. Plant Cell Envrion. 32, 1596–1611 (2009).CAS 
    Article 

    Google Scholar 
    153.Hatch, A. B. Influence of plant litter on the Jarrah forest soils of the Dwellingup region. West. Aust. For. Timber Bur. Leaflet 18 (1955).154.Hayes, P., Turner, B. L., Lambers, H. & Laliberte, E. Foliar nutrient concentrations and resorption efficiency in plants of contrasting nutrient-acquisition strategies along a 2-million-year dune chronosequence. J. Ecol. 102, 396–410 (2013).Article 
    CAS 

    Google Scholar 
    155.Hayes, P. E., Clode, P. L., Oliveira, R. S. & Lambers, H. Proteaceae from phosphorus-impoverished habitats preferentially allocate phosphorus to photosynthetic cells: an adaptation improving phosphorus-use efficiency. Plant Cell Envrion. 41, 605–619 (2018).CAS 
    Article 

    Google Scholar 
    156.Henery, M. L. & Westoby, M. Seed mass and seed nutrient content as predictors of seed output variation between species. Oikos 92, 479–490 (2001).Article 

    Google Scholar 
    157.Hocking, P. J. The nutrition of fruits of two proteaceous shrubs, Grevillea wilsonii and Hakea undulata, from south-western Australia. Aust. J. Bot. 30, 219–230 (1982).CAS 
    Article 

    Google Scholar 
    158.Hocking, P. J. Mineral nutrient composition of leaves and fruits of selected species of Grevillea from southwestern Australia, with special reference to Grevillea leucopteris Meissn. Aust. J. Bot. 34, 155–164 (1986).CAS 
    Article 

    Google Scholar 
    159.Hong, L. T. et al. Plant resources of south east Asia: Timber trees. World biodiversity Database CD rom series (Springer-Verlag Berlin; Heidelberg GmbH; Co. KG, 1999).160.Hopmans, P., Stewart, H. T. L. & Flinn, D. W. Impacts of harvesting on nutrients in a eucalypt ecosystem in southeastern Australia. For. Ecol. Manage. 59, 29–51 (1993).Article 

    Google Scholar 
    161.Huang, G., Rymer, P. D., Duan, H., Smith, R. A. & Tissue, D. T. Elevated temperature is more effective than elevated CO2 in exposing genotypic variation in Telopea speciosissima growth plasticity: implications for woody plant populations under climate change. Glob. Chang. Biol. 21, 3800–3813 (2015).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    162.Hyland, B. P. M., Whiffin, T., Christophel, D., Gray, B. & Elick, R. W. Australian tropical rain forest plants trees, shrubs and vines. (CSIRO Publishing, 2003).163.World Agroforestry Centre (ICRAF). The wood density database. http://www.worldagroforestry.org/output/wood-density-database (2009).164.Ilic, J., Boland, D., McDonald, M., G., D. & Blakemore, P. Woody density phase 1 – State of knowledge. National Carbon Accounting System. Technical Report 18. (Australian Greenhouse Office, Canberra, Australia, 2000).165.Islam, M., Turner, D. W. & Adams, M. A. Phosphorus availability and the growth, mineral composition and nutritive value of ephemeral forbs and associated perennials from the Pilbara, Western Australia. Aust. J. Exp. Agric. 39, 149–159 (1999).Article 

    Google Scholar 
    166.Islam, M. & Adams, M. A. Mineral content and nutritive value of native grasses and the response to added phosphorus in a Pilbara rangeland. Trop. Grassl. 33, 193–200 (1999).
    Google Scholar 
    167.Jordan, G. J. An investigation of long-distance dispersal based on species native to both Tasmania and New Zealand. Aust. J. Bot. 49, 333–340 (2001).Article 

    Google Scholar 
    168.Jordan, G. J., Weston, P. H., Carpenter, R. J., Dillon, R. A. & Brodribb, T. J. The evolutionary relations of sunken, covered, and encrypted stomata to dry habitats in Proteaceae. Am. J. Bot. 95, 521–530 (2008).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    169.Jordan, G. J., Carpenter, R. J., Koutoulis, A., Price, A. & Brodribb, T. J. Environmental adaptation in stomatal size independent of the effects of genome size. New Phytol. 205, 608–617 (2015).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    170.Jordan, G. J. et al. Links between environment and stomatal size through evolutionary time in Proteaceae. Proc. R. Soc. Lond. B Biol. Sci. 287, 20192876 (2020).CAS 

    Google Scholar 
    171.Jurado, E. Diaspore weight, dispersal, growth form and perenniality of central Australian plants. J. Ecol. 79, 811–828 (1991).Article 

    Google Scholar 
    172.Jurado, E. & Westoby, M. Germination biology of selected central Australian plants. Austral Ecol. 17, 341–348 (1992).Article 

    Google Scholar 
    173.Kanowski, J. Ecological determinants of the distribution and abundance of the folivorous marsupials endemic to the rainforests of the Atherton uplands, north Queensland. (James Cook University, Townsville, 1999).174.Keighery, G. Taxonomy of the Calytrix ecalycata complex (Myrtaceae). Nuytsia 15, 261–268 (2004).
    Google Scholar 
    175.Royal Botanic Gardens Kew. Seed Information Database (SID) and Seed Bank Database. http://data.kew.org/sid/ (2019).176.Royal Botanic Gardens Kew. Seed protein data from Seed Information Database (SID) and Seed Bank Database. http://data.kew.org/sid/ (2019).177.Royal Botanic Gardens Kew. Oil content data from Seed Information Database (SID) and Seed Bank Database. http://data.kew.org/sid/ (2019).178.Royal Botanic Gardens Kew. Seed dispersal data from the Seed Information Database (SID) and Seed Bank Database. http://data.kew.org/sid/ (2019).179.Royal Botanic Gardens Kew. Germination data from the Seed Information Database (SID) and Seed Bank Database. http://data.kew.org/sid/ (2019).180.Knox, K. J. E. & Clarke, P. J. Fire severity and nutrient availability do not constrain resprouting in forest shrubs. Plant Ecol. 212, 1967–1978 (2011).Article 

    Google Scholar 
    181.Körner, C. & Cochrane, P. M. Stomatal responses and water relations of Eucalyptus pauciflora in summer along an elevational gradient. Oecologia 66, 443–455 (1985).ADS 
    PubMed 
    Article 

    Google Scholar 
    182.Kooyman, R., Rossetto, M., Cornwell, W. & Westoby, M. Phylogenetic tests of community assembly across regional to continental scales in tropical and subtropical rain forests. Glob. Ecol. Biog. 20, 707–716 (2011).Article 

    Google Scholar 
    183.Kotowska, M. M., Wright, I. J. & Westoby, M. Parenchyma abundance in wood of evergreen trees varies independently of nutrients. Front. Plant. Sci. 11, art86 (2020).Article 

    Google Scholar 
    184.Kuo, J., Hocking, P. & Pate, J. Nutrient reserves in seeds of selected Proteaceous species from South-western Australia. Aust. J. Bot. 30, 231–249 (1982).CAS 
    Article 

    Google Scholar 
    185.Laliberté, E. et al. Experimental assessment of nutrient limitation along a 2-million-year dune chronosequence in the south-western Australia biodiversity hotspot. J. Ecol. 100, 631–642 (2012).Article 
    CAS 

    Google Scholar 
    186.Lambert, M. J. Sulphur relationships of native and exotic tree species. (Macquarie University, Sydney, 1979).187.Lamont, B. B., Groom, P. K. & Cowling, R. M. High leaf mass per area of related species assemblages may reflect low rainfall and carbon isotope discrimination rather than low phosphorus and nitrogen concentrations. Funct. Ecol. 16, 403–412 (2002).Article 

    Google Scholar 
    188.Lamont, B. B., Groom, P. K., Williams, M. & He, T. LMA, density and thickness: recognizing different leaf shapes and correcting for their nonlaminarity. New Phytol. 207, 942–947 (2015).PubMed 
    Article 

    Google Scholar 
    189.Landsberg, J. Dieback of rural eucalypts: response of foliar dietary quality and herbivory to defoliation. Austral Ecol. 15, 89–96 (1990).Article 

    Google Scholar 
    190.Landsberg, J. & Gillieson, D. S. Regional and local variation in insect herbivory, vegetation and soils of eucalypt associations in contrasted landscape positions along a climatic gradient. Aust. J. Ecol. 20, 299–315 (1995).Article 

    Google Scholar 
    191.Lawes, M. J., Adie, H., Russell-Smith, J., Murphy, B. & Midgley, J. J. How do small savanna trees avoid stem mortality by fire? The roles of stem diameter, height and bark thickness. Ecosphere 2, 1–13 (2011).Article 

    Google Scholar 
    192.Lawes, M. J., Richards, A., Dathe, J. & Midgley, J. J. Bark thickness determines fire resistance of selected tree species from fire-prone tropical savanna in north Australia. Plant Ecol. 212, 2057–2069 (2011).Article 

    Google Scholar 
    193.Lawes, M. J., Midgley, J. J. & Clarke, P. J. Costs and benefits of relative bark thickness in relation to fire damage: A savanna/forest contrast. J. Ecol. 101, 517–524 (2012).Article 

    Google Scholar 
    194.Lawson, J. R., Fryirs, K. A. & Leishman, M. R. Data from: Hydrological conditions explain wood density in riparian plants of south-eastern Australia. Dryad Digital Repository https://doi.org/10.5061/dryad.72h45 (2015).195.Laxton, E. Relationship between leaf traits, insect communities and resource availability. (Macquarie University, 2005).196.Lee, M. R. et al. Good neighbors aplenty: fungal endophytes rarely exhibit competitive exclusion patterns across a span of woody habitats. Ecology 100, e02790 (2019).PubMed 
    Article 

    Google Scholar 
    197.Leigh, A. & Nicotra, A. B. Sexual dimorphism in reproductive allocation and water use efficiency in Maireana pyramidata (Chenopodiaceae), a dioecious, semi-arid shrub. Aust. J. Bot. 51, 509–514 (2003).Article 

    Google Scholar 
    198.Leigh, A., Cosgrove, M. J. & Nicotra, A. B. Reproductive allocation in a gender dimorphic shrub: anomalous female investment in Gynatrix pulchella? J. Ecol. 94, 1261–1271 (2006).Article 

    Google Scholar 
    199.Leishman, M. R. & Westoby, M. Classifying plants into groups on the basis of associations of individual traits–Evidence from Australian semi-arid woodlands. J. Ecol. 80, 417–424 (1992).Article 

    Google Scholar 
    200.Leishman, M. R., Westoby, M. & Jurado, E. Correlates of seed size variation: A comparison among five temperate floras. J. Ecol. 83, 517–529 (1995).Article 

    Google Scholar 
    201.Leishman, M. R., Haslehurst, T., Ares, A. & Baruch, Z. Leaf trait relationships of native and invasive plants: community- and global-scale comparisons. New Phytol. 176, 635–643 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    202.Lemmens, R. H. M. J. & Soerjanegara, I. Prosea, Volume 5/1: Timber Trees – Major Commercial Timbers. (Pudoc/Prosea, 1993).203.Lenz, T. I., Wright, I. J. & Westoby, M. Interrelations among pressure-volume curve traits across species and water availability gradients. Physiol. Plant. 127, 423–433 (2006).CAS 
    Article 

    Google Scholar 
    204.Leuning, R., Cromer, R. N. & Rance, S. Spatial distributions of foliar nitrogen and phosphorus in crowns of Eucalyptus grandis. Oecologia 88, 504–510 (1991).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    205.Lewis, J. D. et al. Rising temperature may negate the stimulatory effect of rising CO2 on growth and physiology of Wollemi pine (Wollemia nobilis). Funct. Plant. Bio. 42, 836–850 (2015).CAS 
    Article 

    Google Scholar 
    206.Lim, F. K. S., Pollock, L. J. & Vesk, P. A. The role of plant functional traits in shrub distribution around alpine frost hollows. J. Veg. Sci. 28, 585–594 (2017).Article 

    Google Scholar 
    207.Lord, J. et al. Larger seeds in tropical floras: Consistent patterns independent of growth form and dispersal mode. J. Biogeogr. 24, 205–211 (1997).Article 

    Google Scholar 
    208.Lusk, C. H., Onoda, Y., Kooyman, R. & Gutiurrez-Giron, A. Reconciling species-level vs plastic responses of evergreen leaf structure to light gradients: shade leaves punch above their weight. New Phytol. 186, 429–438 (2010).PubMed 
    Article 

    Google Scholar 
    209.Lusk, C. H., Kelly, J. W. G. & Gleason, S. M. Light requirements of Australian tropical vs. cool-temperate rainforest tree species show different relationships with seedling growth and functional traits. Ann. Bot. 111, 479–488 (2012).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    210.Lusk, C. H., Sendall, K. M. & Clarke, P. J. Seedling growth rates and light requirements of subtropical rainforest trees associated with basaltic and rhyolitic soils. Aust. J. Bot. 62, 48–55 (2014).Article 

    Google Scholar 
    211.Macinnis-Ng, C., McClenahan, K. & Eamus, D. Convergence in hydraulic architecture, water relations and primary productivity amongst habitats and across seasons in Sydney. Funct. Plant. Bio. 31, 429–439 (2004).Article 

    Google Scholar 
    212.Macinnis-Ng, C. M. O., Zeppel, M. J. B., Palmer, A. R. & Eamus, D. Seasonal variations in tree water use and physiology correlate with soil salinity and soil water content in remnant woodlands on saline soils. J. Arid Environ. 129, 102–110 (2016).ADS 
    Article 

    Google Scholar 
    213.Marsh, N. R. & Adams, M. A. Decline of Eucalyptus tereticornis near Bairnsdale, Victoria: insect herbivory and nitrogen fractions in sap and foliage. Aust. J. Bot. 43, 39–49 (1995).Article 

    Google Scholar 
    214.Maslin, B. WATTLE, Interactive Identification of Australian Acacia. Version 2. (Australian Biological Resources Study, Canberra, 2014).215.McCarthy, J. K., Dwyer, J. M. & Mokany, K. A regional-scale assessment of using metabolic scaling theory to predict ecosystem properties. Proc. R. Soc. Lond. B Biol. Sci. 286, 20192221 (2019).
    Google Scholar 
    216.McClenahan, K., Macinnis-Ng, C. & Eamus, D. Hydraulic architecture and water relations of several species at diverse sites around Sydney. Aust. J. Bot. 52, 509–518 (2004).Article 

    Google Scholar 
    217.McGlone, M. S., Richardson, S. J. & Jordan, G. J. Comparative biogeography of New Zealand trees: Species richness, height, leaf traits and range sizes. New Zealand J. Ecol. 34, 137–151 (2010).
    Google Scholar 
    218.McGlone, M. S., Richardson, S. J., Jordan, G. J. & Perry, G. L. W. Is there a “suboptimal” woody species height? A response to Scheffer et al. Trends in Ecol. Evo. 30, 4–5 (2015).Article 

    Google Scholar 
    219.McIntyre, S., Lavorel, S. & Tremont, R. M. Plant life-history attributes: Their relationship to disturbance response in herbaceous vegetation. The J. Ecol. 83, 31–44 (1995).Article 

    Google Scholar 
    220.Meers, T. Role of plant functional traits in determining the response of vegetation to land use change on the Delatite Peninsula, Victoria. (University of Melbourne, 2007).221.Meers, T. L., Bell, T. L., Enright, N. J. & Kasel, S. Role of plant functional traits in determining vegetation composition of abandoned grazing land in north-eastern Victoria, Australia. J. Veg. Sci. 19, 515–524 (2008).Article 

    Google Scholar 
    222.Meers, T. L., Bell, T. L., Enright, N. J. & Kasel, S. Do generalisations of global trade-offs in plant design apply to an Australian sclerophyllous flora? Aust. J. Bot. 58, 257–270 (2010).Article 

    Google Scholar 
    223.Meers, T. L., Kasel, S., Bell, T. L. & Enright, N. J. Conversion of native forest to exotic Pinus radiata plantation: response of understorey plant composition using a plant functional trait approach. For. Ecol. Manage. 259, 399–409 (2010).Article 

    Google Scholar 
    224.Meier, E. The wood database. http://www.wood-database.com/ (2007).225.Laliberté, E. et al. Land-use intensification reduces functional redundancy and response diversity in plant communities. Ecol. Lett. 13, 76–86 (2010).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    226.Milberg, P. & Lamont, B. B. Seed/cotyledon size and nutrient content play a major role in early performance of species on nutrient-poor soils. New Phytol. 137, 665–672 (1997).Article 

    Google Scholar 
    227.Milberg, P., Pérez-Fernández, M. A. & Lamont, B. B. Seedling growth response to added nutrients depends on seed size in three woody genera. J. Ecol. 86, 624–632 (1998).Article 

    Google Scholar 
    228.Mokany, K. & Ash, J. Are traits measured on pot grown plants representative of those in natural communities? J. Veg. Sci. 19, 119–126 (2008).Article 

    Google Scholar 
    229.Mokany, K., Thomson, J. J., Lynch, A. J. J., Jordan, G. J. & Ferrier, S. Linking changes in community composition and function under climate change. Ecol. Appl. 25, 2132–2141 (2015).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    230.Moles, A. T. & Westoby, M. Do small leaves expand faster than large leaves, and do shorter expansion times reduce herbivore damage? Oikos 90, 517–524 (2000).Article 

    Google Scholar 
    231.Moles, A. T., Warton, D. I. & Westoby, M. Seed size and survival in the soil in arid Australia. Austral Ecol. 28, 575–585 (2003).Article 

    Google Scholar 
    232.Moles, A. T. et al. Putting plant resistance traits on the map: A test of the idea that plants are better defended at lower latitudes. New Phytol. 191, 777–788 (2011).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    233.Mooney, H. A., Ferrar, P. J. & Slatyer, R. O. Photosynthetic capacity and carbon allocation patterns in diverse growth forms of Eucalyptus. Oecologia 36, 103–111 (1978).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    234.Moore, A. W., Russell, J. S. & Coaldrake, J. E. Dry matter and nutrient content of a subtropical semiarid forest of Acacia harpophylla F. Muell. (Brigalow). Aust. J. Bot. 15, 11–24 (1967).Article 

    Google Scholar 
    235.Moore, N. A., Camac, J. S. & Morgan, J. W. Effects of drought and fire on resprouting capacity of 52 temperate Australian perennial native grasses. New Phytol. 221, 1424–1433 (2018).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    236.Morgan, H. Root system architecture, water use and rainfall responses of perennial species. (Macquarie University, 2005).237.Muir, A. M., Vesk, P. A. & Hepworth, G. Reproductive trajectories over decadal time-spans after fire for eight obligate-seeder shrub species in south-eastern Australia. Aust. J. Bot. 62, 369–379 (2014).Article 

    Google Scholar 
    238.Munroe, S. E. M. et al. The photosynthetic pathways of plant species surveyed in Australia’s national terrestrial monitoring network. Scientific Data 8, 97 (2021).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    239.National Herbarium of NSW. Trait measurements for NSW rainforest species from PLantNET. http://plantnet.rbgsyd.nsw.gov.au/ (2016).240.Nicholson, A., Prior, L. D., Perry, G. L. W. & Bowman, D. M. J. S. High post-fire mortality of resprouting woody plants in Tasmanian Mediterranean-type vegetation. Int. J. Wildland Fire 26, 532–537 (2017).Article 

    Google Scholar 
    241.Nicolle, D. A classification and census of regenerative strategies in the eucalypts (Angophora, Corymbia and Eucalyptus – Myrtaceae), with special reference to the obligate seeders. Aust. J. Bot. 54, 391–407 (2006).Article 

    Google Scholar 
    242.Nicolle, D. Classification of the Eucalypts (Angophora, Corymbia and Eucalyptus) Version 3. (Currency Creek Arboretum Eucalypt Research, 2018).243.Niinemets, U., Wright, I. J. & Evans, J. R. Leaf mesophyll diffusion conductance in 35 Australian sclerophylls covering a broad range of foliage structural and physiological variation. J. Exp. Bot. 60, 2433–2449 (2009).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    244.Kenny, B., Orscheg, C., Tasker, E., Gill, M. A. & Bradstock, R. NSW Flora Fire Response Database, v2.1. (NSW Department of Planning Industry; Environment, 2014).245.Northern Territory Herbarium. Flora of the Darwin Region Online. http://www.lrm.nt.gov.au/plants-and-animals/herbarium/darwin_flora_online (2014).246.Onoda, Y., Richards, A. E. & Westoby, M. The relationship between stem biomechanics and wood density is modified by rainfall in 32 Australian woody plant species. New Phytol. 185, 493–501 (2009).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    247.O’Reilly-Nugent, A. et al. Measuring competitive impact: Joint‐species modelling of invaded plant communities. J. Ecol. 108, 449–459 (2018).Article 

    Google Scholar 
    248.Osborne, C. P. et al. A global database of C4 photosynthesis in grasses. New Phytol. 204, 441–446 (2014).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    249.Paczkowska G. & Chapman, A.R. The Western Australian flora: A descriptive catalogue. 652 (CALM, Kings Park; Botanic Gardens; Wildflower Society of Western Australia, 2000).250.Palma, E. et al. Functional trait changes in the floras of 11 cities across the globe in response to urbanization. Ecography 40, 875–886 (2017).Article 

    Google Scholar 
    251.Pate, J. S., Rasins, E., Rullo, J. & Kuo, J. Seed nutrient reserves of Proteaceae with special reference to protein bodies and their inclusions. Ann. Bot. 57, 747–770 (1986).CAS 
    Article 

    Google Scholar 
    252.Pearcy, R. W. Photosynthetic gas exchange responses of Australian tropical forest trees in canopy, gap and understory micro-environments. Funct. Ecol. 1, 169–178 (1987).Article 

    Google Scholar 
    253.Peeters, P. J. Correlations between leaf structural traits and the densities of herbivorous insect guilds. Biol. J. Linn. Soc. 77, 43–65 (2002).Article 

    Google Scholar 
    254.Pekin, B. K., Wittkuhn, R. S., Boer, M. M., Macfarlane, C. & Grierson, P. F. Plant functional traits along environmental gradients in seasonally dry and fire-prone ecosystem. J. Veg. Sci. 22, 1009–1020 (2011).Article 

    Google Scholar 
    255.Pickering, C., Green, K., Barros, A. A. & Venn, S. A resurvey of late-lying snowpatches reveals changes in both species and functional composition across snowmelt zones. Alp. Bot. 124, 93–103 (2014).Article 

    Google Scholar 
    256.Pickup, M., Westoby, M. & Basden, A. Dry mass costs of deploying leaf area in relation to leaf size. Funct. Ecol. 19, 88–97 (2005).Article 

    Google Scholar 
    257.Pollock, L. J., Morris, W. K. & Vesk, P. A. The role of functional traits in species distributions revealed through a hierarchical model. Ecography 35, 716–725 (2011).Article 

    Google Scholar 
    258.Pollock, L. J. et al. Combining functional traits, the environment and multiple surveys to understand semi-arid tree distributions. J. Veg. Sci. 29, 967–977 (2018).Article 

    Google Scholar 
    259.Prior, L. D., Eamus, D. & Bowman, D. M. J. S. Leaf attributes in the seasonally dry tropics: A comparison of four habitats in northern Australia. Funct. Ecol. 17, 504–515 (2003).Article 

    Google Scholar 
    260.Prior, L. D., Bowman, D. M. J. S. & Eamus, D. Seasonal differences in leaf attributes in Australian tropical tree species: family and habitat comparisons. Funct. Ecol. 18, 707–718 (2004).Article 

    Google Scholar 
    261.Prior, L. D., Williamson, G. J. & Bowman, D. M. J. S. Impact of high-severity fire in a Tasmainian dry eucalypt forest. Aust. J. Bot. 64, 193–205 (2016).Article 

    Google Scholar 
    262.Oxford Forestry Institute. Prospect: The wood database. http://dps.plants.ox.ac.uk/ofi/prospect/index.htm (2009).263.Royal Botanic Gardens Kew. Seed Information Database (SID). http://data.kew.org/sid/ (2014).264.Royal Botanic Gardens Sydney. PLantNET. http://plantnet.rbgsyd.nsw.gov.au/search/simple.htm (2014).265.Royal Botanic Gardens Sydney. PLantNET: NSW flora online. http://plantnet.rbgsyd.nsw.gov.au/ (2014).266.Read, J. & Sanson, G. D. Characterizing sclerophylly: the mechanical properties of a diverse range of leaf types. New Phytol. 160, 81–99 (2003).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    267.Read, J., Sanson, G. D. & Lamont, B. B. Leaf mechanical properties in sclerophyll woodland and shrubland on contrasting soils. Plant Soil 276, 95–113 (2005).CAS 
    Article 

    Google Scholar 
    268.Reid, J. B., Hill, R., Brown, M. & and M. Hovenden. Vegetation of Tasmania. 456 (1999).269.Reynolds, V. A., Anderegg, L. D. L., Loy, X., HilleRisLambers, J. & Mayfield, M. M. Unexpected drought resistance strategies in seedlings of four Brachychiton species. Tree Physiol. 38, 664–677 (2017).Article 
    CAS 

    Google Scholar 
    270.Rice, K. J., Matzner, S. L., Byer, W. & Brown, J. R. Patterns of tree dieback in Queensland, Australia: The importance of drought stress and the role of resistance to cavitation. Oecologia 139, 190–198 (2004).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    271.Richards, A. E. et al. Physiological profiles of restricted endemic plants and their widespread congenors in the North Queensland wet tropics, Australia. Biol. Conserv. 111, 41–52 (2003).Article 

    Google Scholar 
    272.Roderick, M. L., Berry, S. L. & Noble, I. R. The relationship between leaf composition and morphology at elevated CO2 concentrations. New Phytol. 143, 63–72 (1999).Article 

    Google Scholar 
    273.Roderick, M. L. & Cochrane, M. J. On the conservative nature of the leaf mass-area relationship. Ann. Bot. 89, 537–542 (2002).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    274.Rosell, J. A., Gleason, S., Mendez-Alonzo, R., Chang, Y. & Westoby, M. Bark functional ecology: Evidence for tradeoffs, functional coordination, and environment producing bark diversity. New Phytol. 201, 486–497 (2014).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    275.Rye, B. L. A revision of south-western Australian species of Micromyrtus (Myrtaceae) with five antisepalous ribs on the hypanthium. Nuytsia 15, 101–122 (2002).
    Google Scholar 
    276.Rye, B. L. A partial revision of the south-western Australian species of Micromyrtus (Myrtaceae: Chamelaucieae). Nuytsia 16, 117–147 (2006).
    Google Scholar 
    277.Rye, B. L. Reinstatement of the Western Australian genus Oxymyrrhine (Myrtaceae: Chamelaucieae) with three new species. Nuytsia 19, 149–165 (2009).
    Google Scholar 
    278.Rye, B. L. A revision of the Micromyrtus racemosa complex (Myrtaceae: Chamelaucieae) of south-western Australia. Nuytsia 20, 37–56 (2010).
    Google Scholar 
    279.Rye, B. L., Wilson, P. G. & Keighery, G. J. A revision of the species of Hypocalymma (Myrtaceae: Chamelaucieae) with smooth or colliculate seeds. Nuytsia 23, 283–312 (2013).
    Google Scholar 
    280.Rye, B. L. An update to the taxonomy of some western Australian genera of Myrtaceae tribe Chamelaucieae. 1. Calytrix. Nuytsia 23, 483–501 (2013).
    Google Scholar 
    281.Rye, B. L. A revision of the south-western Australian genus Babingtonia (Myrtaceae: Chamelaucieae). Nuytsia 25, 219–250 (2015).
    Google Scholar 
    282.Jessop, J. P. & Toelken, H. R. Flora of South Australia, 4th edition, 4 vols. (Government Printer, Adelaide, 1986).283.Sams, M. A. et al. Landscape context explains changes in the functional diversity of regenerating forests better than climate or species richness. Glob. Ecol. Biog. 26, 1165–1176 (2017).Article 

    Google Scholar 
    284.Sauquet, H. et al. The ancestral flower of angiosperms and its early diversification. Nat. Commun. 8, 1–10 (2017).Article 
    CAS 

    Google Scholar 
    285.Schmidt, S. & Stewart, G. R. Waterlogging and fire impacts on nitrogen availability and utilization in a subtropical wet heathland (wallum). Plant Cell Envrion. 20, 1231–1241 (1997).Article 

    Google Scholar 
    286.Schmidt, S. & Stewart, G. R. d15N values of tropical savanna and monsoon forest species reflect root specialisations and soil nitrogen status. Oecologia 134, 569–577 (2003).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    287.Schmidt, S., Lamble, R. E., Fensham, R. J. & Siddique, I. Effect of woody vegetation clearing on nutrient and carbon relations of semi-arid dystrophic savanna. Plant Soil 331, 79–90 (2009).Article 
    CAS 

    Google Scholar 
    288.Schulze, E., Kelliher, F. M., Körner, C., Lloyd, J. & Leuning, R. Relationships among maximum stomatal conductance, ecosystem surface conductance, carbon assimilation rate, and plant nitrogen nutrition: A global ecology scaling exercise. Annu. Rev. Ecol. Syst. 25, 629–662 (1994).Article 

    Google Scholar 
    289.Schulze, E.-D. et al. Carbon and nitrogen isotope discrimination and nitrogen nutrition of trees along a rainfall gradient in northern Australia. Aust. J. Plant. Physiol. 25, 413–425 (1998).
    Google Scholar 
    290.Schulze, E.-D., Turner, N. C., Nicolle, D. & Schumacher, J. Species differences in carbon isotope ratios, specific leaf area and nitrogen concentrations in leaves of Eucalyptus growing in a common garden compared with along an aridity gradient. Physiol. Plant. 127, 434–444 (2006).CAS 
    Article 

    Google Scholar 
    291.Schulze, E.-D., Turner, N. C., Nicolle, D. & Schumacher, J. Leaf and wood carbon isotope ratios, specific leaf areas and wood growth of Eucalyptus species across a rainfall gradient in Australia. Tree Physiol. 26, 479–492 (2006).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    292.Turner, N. C., Schulze, E.-D., Nicolle, D., Schumacher, J. & Kuhlmann, I. Annual rainfall does not directly determine the carbon isotope ratio of leaves of Eucalyptus species. Physiol. Plant. 132, 440–445 (2008).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    293.Schulze, E. D. et al. Stable carbon and nitrogen isotope ratios of Eucalyptus and Acacia species along a seasonal rainfall gradient in Western Australia. Trees 28, 1125–1135 (2014).CAS 
    Article 

    Google Scholar 
    294.Scott, A. J. Vegetation recovery and recruitment processes in south-eastern Australian semi-arid old fields. (La Trobe University, 2010).295.Sendall, K. M., Lusk, C. H. & Reich, P. B. Trade-offs in juvenile growth potential vs. shade tolerance among subtropical rain forest trees on soils of contrasting fertility. Funct. Ecol. 30, 845–855 (2015).Article 

    Google Scholar 
    296.Seng, O. D. Specific gravity of Indonesian Woods and its significance for practical use. (FPRDC Forestry Department, Bogor, Indonesia, 1951).297.Sjöström, A. & Gross, C. L. Life-history characters and phylogeny are correlated with extinction risk in the Australian angiosperms. J. Biogeogr. 33, 271–290 (2006).Article 

    Google Scholar 
    298.Smith, B. Community-level Convergence and Community Structure of temperate Nothofagus forests. (University of Otago, Dunedin, New Zealand, 1996).299.Smith, R. A., Lewis, J. D., Ghannoum, O. & Tissue, D. T. Leaf structural responses to pre-industrial, current and elevated atmospheric CO2 and temperature affect leaf function in Eucalyptus sideroxylon. Funct. Plant. Bio. 39, 285–296 (2012).CAS 
    Article 

    Google Scholar 
    300.Soliveres, S., Eldridge, D. J., Hemmings, F. & Maestre, F. T. Nurse plant effects on plant species richness in drylands: The role of grazing, rainfall and species specificity. Perspect. Plant Ecol. Evol. Systs. 14, 402–410 (2012).Article 

    Google Scholar 
    301.Soper, F. M. et al. Natural abundance (delta15N) indicates shifts in nitrogen relations of woody taxa along a savanna-woodland continental rainfall gradient. Oecologia 178, 297–308 (2014).ADS 
    PubMed 
    Article 

    Google Scholar 
    302.Specht, R. L. et al. Mediterranean-type ecosystems: A data source book. 248 (Springer, 1988).303.Specht, R. L. & Rundel, P. W. Sclerophylly and foliar nutrient status of Mediterranean-climate plant communities in southern Australia. Aust. J. Bot. 38, 459–474 (1990).Article 

    Google Scholar 
    304.Sperry, J. S., Hacke, U. G., Feild, T. S., Sano, Y. & Sikkema, E. H. Hydraulic consequences of vessel evolution in Angiosperms. Int. J. Plant Sci. 168, 1127–1139 (2007).Article 

    Google Scholar 
    305.Staples, T., Dwyer, J. M., England, J. R. & Mayfield, M. M. Productivity does not correlate with species and functional diversity in Australian reforestation plantings across a wide climate gradient. Glob. Ecol. Biog. 28, 1417–1429 (2019).Article 

    Google Scholar 
    306.Stewart, G., Turnbull, M., Schmidt, S. & Erskine, P. 13C natural abundance in plant communities along a rainfall gradient: a biological integrator of water availability. Funct. Plant. Bio. 22, 51–55 (1995).Article 

    Google Scholar 
    307.Stock, W. D., Pate, J. S. & Rasins, E. Seed developmental patterns in Banksia attenuata R. Br. and B. laricina C. Gardner in relation to mechanical defence costs. New Phytol. 117, 109–114 (1991).CAS 
    Article 

    Google Scholar 
    308.Tait, C. J., Daniels, C. B. & Hill, R. S. Changes in species assemblages within the Adelaide metropolitan area, Australia, 1836–2002. Ecol. Appl. 15, 346–359 (2005).Article 

    Google Scholar 
    309.Taseski, G., Keith, D. A., Dalrymple, R. L. & Cornwell, W. K. Shifts in fine root traits within and among species along a small-scale hydrological gradient. (University of New South Wales, 2017).310.Taylor, D. & Eamus, D. Coordinating leaf functional traits with branch hydraulic conductivity: Resource substitution and implications for carbon gain. Tree Physiol. 28, 1169–1177 (2008).PubMed 
    Article 

    Google Scholar 
    311.Thomas, F. M. & Vesk, P. A. Growth races in The Mallee: Height growth in woody plants examined with a trait-based model. Austral Ecol. 42, 790–800 (2017).Article 

    Google Scholar 
    312.Thomas, F. M. & Vesk, P. A. Are trait-growth models transferable? Predicting multi-species growth trajectories between ecosystems using plant functional traits. PLoS One 12, e0176959 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    313.Thompson, I. R. Morphometric analysis and revision of eastern Australian Hovea (Brongniartieae-Fabaceae). Aust. Syst. Bot. 14, 1–99 (2001).Article 

    Google Scholar 
    314.Tasmanian Herbarium. Flora of Tasmania Online. http://www.tmag.tas.gov.au/floratasmania (2009).315.Tng, D. Y. P., Jordan, G. J. & Bowman, D. M. J. S. Plant traits demonstrate that temperate and tropical giant Eucalypt forests are ecologically convergent with rainforest not savanna. PLoS One 8, e84378 (2013).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    316.Toelken, H. R. A revision of the genus Kunzea (Myrtaceae) I. The western Australian section Zeanuk. J. Adel. Bot. Gard. 17, 29–106 (1996).
    Google Scholar 
    317.Tomlinson, K. W. et al. Biomass partitioning and root morphology of savanna trees across a water gradient. J. Ecol. 100, 1113–1121 (2012).Article 

    Google Scholar 
    318.Tomlinson, K. W. et al. Leaf adaptations of evergreen and deciduous trees of semi-arid and humid savannas on three continents. J. Ecol. 101, 430–440 (2013).Article 

    Google Scholar 
    319.Tomlinson, K. W. et al. Seedling growth of savanna tree species from three continents under grass competition and nutrient limitation in a greenhouse experiment. J. Ecol. 107, 1051–1066 (2019).Article 

    Google Scholar 
    320.Tremont, R. M. Life-history attributes of plants in grazed and ungrazed grasslands on the Northern Tablelands of New South Wales. Aust. J. Bot. 42, 511–530 (1994).Article 

    Google Scholar 
    321.Trudgen, M. E. & Rye, B. L. Astus, a new western Australian genus of Myrtaceae with heterocarpidic fruits. Nuytsia 14, 495–512 (2005).
    Google Scholar 
    322.Trudgen, M. E. & Rye, B. L. An update to the taxonomy of some western Australian genera of Myrtaceae tribe Chamelaucieae. 2. Cyathostemon. Nuytsia 24, 7–16 (2014).
    Google Scholar 
    323.Turner, J. & Lambert, M. J. Nutrient cycling within a 27-year-old Eucalyptus grandis plantation in New South Wales. For. Ecol. Manage. 6, 155–168 (1983).CAS 
    Article 

    Google Scholar 
    324.Turner, N. C., Schulze, E.-D., Nicolle, D. & Kuhlmann, I. Growth in two common gardens reveals species by environment interaction in carbon isotope discrimination of Eucalyptus. Tree Physiol. 30, 741–747 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    325.Veneklaas, E. J. & Poot, P. Seasonal patterns in water use and leaf turnover of different plant functional types in a species-rich woodland, south-western Australia. Plant Soil 257, 295–304 (2003).CAS 
    Article 

    Google Scholar 
    326.Venn, S. E., Green, K., Pickering, C. M. & Morgan, J. W. Using plant functional traits to explain community composition across a strong environmental filter in Australian alpine snowpatches. Plant Ecol. 212, 1491–1499 (2011).Article 

    Google Scholar 
    327.Venn, S., Pickering, C. & Green, K. Spatial and temporal functional changes in alpine summit vegetation are driven by increases in shrubs and graminoids. AoB Plants 6, plu008 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    328.Vesk, P. A., Leishman, M. R. & Westoby, M. Simple traits do not predict grazing response in Australian dry shrublands and woodlands. J. Appl. Ecol. 41, 22–31 (2004).Article 

    Google Scholar 
    329.Vesk, P. A. & Yen, J. D. L. Plant resprouting: How many sprouts and how deep? Flexible modelling of multispecies experimental disturbances. Perspect. Plant Ecol. Evol. Systs. 41, 125497 (2019).Article 

    Google Scholar 
    330.Vlasveld, C., O’Leary, B., Udovicic, F. & Burd, M. Leaf heteroblasty in eucalypts: biogeographic evidence of ecological function. Aust. J. Bot. 66, 191–201 (2018).Article 

    Google Scholar 
    331.Western Australian Herbarium. FloraBase: The Western Australian flora. http://florabase.dpaw.wa.gov.au (1998).332.Western Australian Herbarium. FloraBase: The Western Australian flora. http://florabase.dpaw.wa.gov.au/ (2016).333.Warren, C. R., Tausz, M. & Adams, M. A. Does rainfall explain variation in leaf morphology and physiology among populations of red ironbark (Eucalyptus sideroxylon subsp. tricarpa) grown in a common garden? Tree Physiol. 25, 1369–1378 (2005).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    334.Warren, C. R., Dreyer, E., Tausz, M. & Adams, M. A. Ecotype adaptation and acclimation of leaf traits to rainfall in 29 species of 16-year-old Eucalyptus at two common gardens. Funct. Ecol. 20, 929–940 (2006).Article 

    Google Scholar 
    335.Weerasinghe, L. K. et al. Canopy position affects the relationships between leaf respiration and associated traits in a tropical rainforest in Far North Queensland. Tree Physiol. 34, 564–584 (2014).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    336.Wells, J. A. Phylogeny and inter-relations of ecological traits and seed dispersal in rainforest plants: Exploring aspects of functional diversity in primary and secondary rainforests in Australia’s Wet Tropics. (University of Queensland, 2012).337.Westman, W. E. & Roggers, R. V. Nutrient stocks in a subtropical eucalypt forest, North Stradbroke Island. Austral Ecol. 2, 447–460 (1977).Article 

    Google Scholar 
    338.Westoby, M. et al. Seed size and plant growth form as factors in dispersal spectra. Ecology 71, 1307–1315 (1990).Article 

    Google Scholar 
    339.Westoby, M. & Wright, I. J. The leaf size – twig size spectrum and its relationship to other important spectra of variation among species. Oecologia 135, 621–628 (2003).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    340.Wheeler, J. R., Marchant, N. G. & Lewington, M. Flora of the south west: Bunbury, Augusta, Denmark. (Australian Biological Resources Study; University of Western Australia Press, 2002).341.White, M., Sinclair, S. & Frood, D. Victorian Vital Attributes Database. (Department of Environment, Land, Water; Planning, Victoria, 2020).342.Williams, N. S. G., Morgan, J. W., McDonnell, M. J. & McCarthy, M. A. Plant traits and local extinctions in natural grasslands along an urban-rural gradient. J. Ecol. 93, 1203–1213 (2005).Article 

    Google Scholar 
    343.Wills, J. et al. Tree leaf trade-offs are stronger for sub-canopy trees: leaf traits reveal little about growth rates in canopy trees. Ecol. Appl. 28, 1116–1125 (2018).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    344.Wilson, P. G. & Rowe, R. A revision of the Indigofereae (Fabaceae) in Australia. 2. Indigofera species with trifoliolate and alternately pinnate leaves. Telopea 12, 293–307 (2008).Article 

    Google Scholar 
    345.Wright, I. J. et al. A survey of seed and seedling characters in 1744 Australian dicotyledon species: Cross-species trait correlations and correlated trait-shifts within evolutionary lineages. Biol. J. Linn. Soc. 69, 521–547 (2000).Article 

    Google Scholar 
    346.Wright, I. J., Reich, P. B. & Westoby, M. Strategy shifts in leaf physiology, structure and nutrient content between species of high- and low-rainfall and high- and low-nutrient habitats. Funct. Ecol. 15, 423–434 (2001).Article 

    Google Scholar 
    347.Wright, I. J. & Westoby, M. Leaves at low versus high rainfall: Coordination of structure, lifespan and physiology. New Phytol. 155, 403–416 (2002).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    348.Wright, I. J., Westoby, M. & Reich, P. B. Convergence towards higher leaf mass per area in dry and nutrient-poor habitats has different consequences for leaf life span. J. Ecol. 90, 534–543 (2002).Article 

    Google Scholar 
    349.Wright, I. J., Falster, D. S., Pickup, M. & Westoby, M. Cross-species patterns in the coordination between leaf and stem traits, and their implications for plant hydraulics. Physiol. Plant. 127, 445–456 (2006).CAS 
    Article 

    Google Scholar 
    350.Wright, I. J. et al. Stem diameter growth rates in a fire-prone savanna correlate with photosynthetic rate and branch-scale biomass allocation, but not specific leaf area. Austral Ecol. 44, 339–350 (2018).Article 

    Google Scholar 
    351.Yates, C. J. et al. Mallee woodlands and shrublands: the mallee, muruk/muert and maalok vegetation of Southern Australia. in Australian Vegetation (Cambridge University Press, 2017).352.Zanne, A. E. et al. Data from: Towards a worldwide wood economics spectrum. Dryad https://doi.org/10.5061/dryad.234 (2009).353.Zieminska, K., Butler, D. W., Gleason, S. M., Wright, I. J. & Westoby, M. Fibre wall and lumen fractions drive wood density variation across 24 Australian angiosperms. AoB Plants 5, plt046 (2013).PubMed Central 
    Article 
    CAS 

    Google Scholar 
    354.Zieminska, K., Westoby, M. & Wright, I. J. Broad anatomical variation within a narrow wood density range – A study of twig wood across 69 Australian Angiosperms. PLoS One 10, e0124892 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    355.R Core Team. R: A language and environment for statistical computing. (R Foundation for Statistical Computing, 2020).356.Wickham, H. et al. Welcome to the tidyverse. Journal of Open Source Software 4, 1686 (2019).ADS 
    Article 

    Google Scholar 
    357.Stephens, J. Yaml: Methods to convert r data to YAML and back (r package version 2.1. 13). (2014).358.FitzJohn, R. Remake: Make-like build management. R package version 0.2.0. (2016).359.Xie, Y. Dynamic documents with R and Knitr. (2015).360.Allaire, J. et al. Rmarkdown: Dynamic documents for R. R package version 0.5.1. (2015).361.CHAH. Australian Plant Name Index (continuously updated), Centre of Australian National Biodiversity Research. (https://www.biodiversity.org.au/nsl/services/apni (14/05/2020), 2020).362.Chamberlain, S. A. & Szöcs, E. Taxize: Taxonomic search and retrieval in R. F1000Res. 2, 191 (2013).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    363.Falster, D. et al. AusTraits: a curated plant trait database for the Australian flora. Zenodo https://doi.org/10.5281/zenodo.3568417 (2021).364.Wilkinson, M. D. et al. The FAIR guiding principles for scientific data management and stewardship. Sci. Data 3 (2016).365.Falster, D. S., FitzJohn, R. G., Pennell, M. W. & Cornwell, W. K. Datastorr: A workflow and package for delivering successive versions of ‘evolving data’ directly into R. GigaScience 8, giz035 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    366.Smith, S. A. & Brown, J. W. Constructing a broadly inclusive seed plant phylogeny. Am. J. Bot. 105, 302–314 (2018).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    367.Jin, Y. V.PhyloMaker: Make phylogenetic hypotheses for vascular plants, etc.. R package version 0.1.0. (2020).368.Yu, G., Smith, D. K., Zhu, H., Guan, Y. & Lam, T. T.-Y. Gtree: An r package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods in Ecol. Evo. 8, 28–36 (2017).Article 

    Google Scholar 
    369.Stefan, V. & Levin, S. Plotbiomes: Plot Whittaker biomes with ggplot2. R package version 0.0.0.9001. (2020).370.Whittaker, R. H. Communities and ecosystems. (MacMillan Publishers, 1975).371.Fick, S. E. & Hijmans, R. J. WorldClim 2: New 1-km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37, 4302–4315 (2017).Article 

    Google Scholar  More

  • in

    Exacerbated drought impacts on global ecosystems due to structural overshoot

    1.Allen, C. D. et al. A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For. Ecol. Manag. 259, 660–684 (2010).
    Google Scholar 
    2.Ciais, P. et al. Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437, 529–533 (2005).CAS 

    Google Scholar 
    3.Zhao, M. & Running, S. W. Drought-induced reduction in global terrestrial net primary production from 2000 through 2009. Science 329, 940–943 (2010).CAS 

    Google Scholar 
    4.Orth, R. & Destouni, G. Drought reduces blue-water fluxes more strongly than green-water fluxes in Europe. Nat. Commun. 9, 3602 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    5.Doughty, C. E. et al. Drought impact on forest carbon dynamics and fluxes in Amazonia. Nature 519, 78–82 (2015).CAS 

    Google Scholar 
    6.Schwalm, C. R. et al. Reduction in carbon uptake during turn of the century drought in western North America. Nat. Geosci. 5, 551–556 (2012).CAS 

    Google Scholar 
    7.Bastos, A. et al. Direct and seasonal legacy effects of the 2018 heat wave and drought on European ecosystem productivity. Sci. Adv. 6, eaba2724 (2020).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    8.Wolf, S. et al. Warm spring reduced carbon cycle impact of the 2012 US summer drought. Proc. Natl Acad. Sci. USA 113, 5880–5885 (2016).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    9.Jump, A. S. et al. Structural overshoot of tree growth with climate variability and the global spectrum of drought‐induced forest dieback. Glob. Change Biol. 23, 3742–3757 (2017).
    Google Scholar 
    10.Buermann, W. et al. Widespread seasonal compensation effects of spring warming on northern plant productivity. Nature 562, 110–114 (2018).CAS 

    Google Scholar 
    11.Goulden, M. L. & Bales, R. C. California forest die-off linked to multi-year deep soil drying in 2012–2015 drought. Nat. Geosci. 12, 632–637 (2019).CAS 

    Google Scholar 
    12.West, M. & Harrison, J. Bayesian Forecasting and Dynamic Models (Springer, 1997).13.Pinzon, J. E. & Tucker, C. J. A non-stationary 1981–2012 AVHRR NDVI3g time series. Remote Sens. 6, 6929–6960 (2014).
    Google Scholar 
    14.Nemani, R. R. Climate-driven increases in global terrestrial net primary production from 1982 to 1999. Science 300, 1560–1563 (2003).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    15.Zhang, X., Friedl, M. A., Schaaf, C. B. & Strahler, A. H. Climate controls on vegetation phenological patterns in northern mid and high latitudes inferred from MODIS data. Glob. Change Biol. 10, 1133–1145 (2004).
    Google Scholar 
    16.Zeng, Z. et al. Impact of earth greening on the terrestrial water cycle. J. Clim. 31, 2633–2650 (2018).
    Google Scholar 
    17.Vicente-Serrano, S. M. et al. Response of vegetation to drought time-scales across global land biomes. Proc. Natl Acad. Sci. USA 110, 52–57 (2013).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    18.Anderegg, W. R. L. et al. Hydraulic diversity of forests regulates ecosystem resilience during drought. Nature 561, 538–541 (2018).CAS 

    Google Scholar 
    19.Isbell, F. et al. Biodiversity increases the resistance of ecosystem productivity to climate extremes. Nature 526, 574–577 (2015).CAS 
    PubMed 

    Google Scholar 
    20.Lian, X. et al. Partitioning global land evapotranspiration using CMIP5 models constrained by observations. Nat. Clim. Change 8, 640–646 (2018).
    Google Scholar 
    21.Zscheischler, J. et al. Future climate risk from compound events. Nat. Clim. Change 8, 469–477 (2018).
    Google Scholar 
    22.Zscheischler, J. et al. A typology of compound weather and climate events. Nat. Rev. Earth Environ. 1, 333–347 (2020).
    Google Scholar 
    23.Zhou, S., Zhang, Y., Williams, A. P. & Gentine, P. Projected increases in intensity, frequency, and terrestrial carbon costs of compound drought and aridity events. Sci. Adv. 5, eaau5740 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    24.Hersbach, H. et al. The ERA5 global reanalysis. Q. J. R. Meteorol. Soc. 146, 1999–2049 (2020).
    Google Scholar 
    25.Sungmin, O. & Orth, R. Global soil moisture data derived through machine learning trained with in-situ measurements. Sci. Data 8, 170 (2021).
    Google Scholar 
    26.Pendergrass, A. G. et al. Flash droughts present a new challenge for subseasonal-to-seasonal prediction. Nat. Clim. Change 10, 191–199 (2020).
    Google Scholar 
    27.Otkin, J. A. et al. Flash droughts: a review and assessment of the challenges imposed by rapid-onset droughts in the United States. Bull. Am. Meteorol. Soc. 99, 911–919 (2018).
    Google Scholar 
    28.Lian, X. et al. Summer soil drying exacerbated by earlier spring greening of northern vegetation. Sci. Adv. 6, eaax0255 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    29.Green, J. K. et al. Regionally strong feedbacks between the atmosphere and terrestrial biosphere. Nat. Geosci. 10, 410–414 (2017).CAS 

    Google Scholar 
    30.Keenan, T. F. & Richardson, A. D. The timing of autumn senescence is affected by the timing of spring phenology: implications for predictive models. Glob. Change Biol. 21, 2634–2641 (2015).
    Google Scholar 
    31.Zani, D., Crowther, T. W., Mo, L., Renner, S. S. & Zohner, C. M. Increased growing-season productivity drives earlier autumn leaf senescence in temperate trees. Science 370, 1066–1071 (2020).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    32.Buitenwerf, R., Rose, L. & Higgins, S. I. Three decades of multi-dimensional change in global leaf phenology. Nat. Clim. Change 5, 364–368 (2015).
    Google Scholar 
    33.Douville, H., Ribes, A., Decharme, B., Alkama, R. & Sheffield, J. Anthropogenic influence on multidecadal changes in reconstructed global evapotranspiration. Nat. Clim. Change 3, 59–62 (2013).
    Google Scholar 
    34.Asrar, G., Fuchs, M., Kanemasu, E. T. & Hatfield, J. L. Estimating absorbed photosynthetic radiation and leaf area index from spectral reflectance in wheat. Agron. J. 76, 300–306 (1984).
    Google Scholar 
    35.Chen, J. M. & Cihlar, J. Retrieving leaf area index of boreal conifer forests using Landsat TM images. Remote Sens. Environ. 55, 153–162 (1996).
    Google Scholar 
    36.Piao, S. et al. Characteristics, drivers and feedbacks of global greening. Nat. Rev. Earth Environ. 1, 14–27 (2020).
    Google Scholar 
    37.Becker, A. et al. A description of the global land-surface precipitation data products of the Global Precipitation Climatology Centre with sample applications including centennial (trend) analysis from 1901–present. Earth Syst. Sci. Data 5, 71–99 (2013).
    Google Scholar 
    38.Sun, Q. et al. A review of global precipitation data sets: data sources, estimation, and intercomparisons. Rev. Geophys. 56, 79–107 (2018).
    Google Scholar 
    39.Harris, I., Osborn, T. J., Jones, P. & Lister, D. Version 4 of the CRU TS monthly high-resolution gridded multivariate climate dataset. Sci. Data 7, 109 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    40.Vicente-Serrano, S. M., Beguería, S. & López-Moreno, J. I. A multiscalar drought index sensitive to global warming: the standardized precipitation evapotranspiration index. J. Clim. 23, 1696–1718 (2010).
    Google Scholar 
    41.Harrison, P. J. & Stevens, C. F. Bayesian forecasting. J. R. Stat. Soc. B 38, 205–247 (1976).
    Google Scholar 
    42.Liu, Y., Kumar, M., Katul, G. G. & Porporato, A. Reduced resilience as an early warning signal of forest mortality. Nat. Clim. Change 9, 880–885 (2019).
    Google Scholar 
    43.Humphrey, V., Gudmundsson, L. & Seneviratne, S. I. Assessing global water storage variability from grace: trends, seasonal cycle, subseasonal anomalies and extremes. Surv. Geophys. 37, 357–395 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    44.Schwalm, C. R. et al. Global patterns of drought recovery. Nature 548, 202–205 (2017).CAS 

    Google Scholar  More

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    Spatial frameworks for robust estimation of yield gaps

    Yield definitionsYield potential (Yp; megagrams per harvested hectare) is defined as the yield of a cultivar in an environment to which it is adapted, when grown with sufficient water and nutrients in the absence of abiotic and biotic stress40. In irrigated fields, Yp is determined by solar radiation, temperature, atmospheric CO2 concentration and management practices that influence crop cycle duration and light interception, such as sowing date, cultivar maturity and plant density. In rainfed systems where water supply from stored soil water at sowing and in-season precipitation is not enough to meet crop water requirements, water-limited Yp (Yw) is determined by water supply amount and its distribution during the growing season, as well as by soil properties influencing the crop–water balance, such as the rootable soil depth, texture and terrain slope. Actual yield is defined as the average grain yield (megagrams per harvested hectare) obtained by farmers for a given crop with a given water regime. The difference between Yp (or Yw) and farmer actual yield is known as the yield gap11. In the case of irrigated crops, Yp is the proper benchmark to estimate yield gaps, while Yw is the meaningful benchmark for rainfed crops. With good, cost-effective crop management, reaching 70–80% of Yp (or Yw) is a reasonable target for farmers with good access to markets, inputs and extension services, which is usually referred to as ‘attainable yield’41,42. Beyond this yield level, the small return to extra input requirement and labour does not justify the associated financial and environmental costs and level of sophistication in crop and soil management practices.Sources of Yp data derived from top-down and bottom-up approachesWe retrieved data generated from two initiatives following a top-down approach: (1) the GAEZ (http://www.fao.org/nr/gaez/en/; refs. 18,19) and (2) the AgMIP (https://agmip.org/data-and-tools-updated/; refs. 20,21). As the bottom-up approach, we used results from the GYGA (www.yieldgap.org; refs. 11,31,43). The main features of these databases are summarized elsewhere (Supplementary Table 1 and Supplementary Section 1). In the process of selecting the specific dataset, we explicitly attempted to reduce biases in the comparisons to the extent this was possible. For example, in all cases, we used simulations that meet the yield definitions provided in the previous section. We also tried to be consistent in terms of the time period for which Yp (or Yw) was simulated; however, this was not always possible, because while GAEZ and AgMIP use weather datasets that cover the time period between 1961 and 1990 and between 1980 and 2010, respectively, GYGA uses more recent weather data (Supplementary Table 1). Similarly, comparisons between databases were limited to those regions for which there were estimates of Yp (or Yw) for each of the top-down and bottom-up approaches. More detailed information about the three approaches can be found in Supplementary Section 1. We acknowledge that, when assessing different approaches, it is conceivable that there would be an inherent bias depending on who performs it and his/her preference. Although the authors of this current study have all contributed to the development of GYGA, we have maintained neutrality when conducting the analysis and made inferences solely based on the results shown here, avoiding any inherent bias. Additionally, methods and data sources are fully documented and publicly accessible for other researchers who may be interested in replicating our comparison.Comparison of bottom-up and top-down approaches at different spatial levelsComparison of the three databases needs to account for the different spatial resolution at which the data are reported (grid in GAEZ and AgMIP versus buffer in GYGA). In the present study, we compared Yp (or Yw) among the three databases at three spatial levels: local (also referred to as buffer), climate zone (CZ) and country (or subcontinent). An example of the three spatial levels evaluated in this study as well as the Yw estimated by each of the three databases for rainfed maize is shown in Extended Data Fig. 4. We note that buffer is the lowest spatial level at which Yp and Yw are reported in GYGA. For a country such as the United States, where maize production is concentrated on flat geographic areas, the average size of buffers and CZs selected by GYGA is 17,000 and 60,000 km2, respectively; the size is smaller for countries with greater terrain and climate heterogeneity, such as Ethiopia, where the average size of buffers and CZs selected for maize by GYGA is a respective 4,000 and 21,000 km2, or for smaller countries, such as in Europe.The GYGA already provides estimates of Yp (or Yw) and yield gaps at those three spatial levels. Following a bottom-up approach, GYGA estimates the Yp (or Yw) at the buffer level based on the Yp (or Yw) simulated for each crop cycle and soil type (within a given buffer) and their associated harvested area (within that same buffer) using a weighted average. Subsequently, Yp (or Yw) at buffer levels are upscaled to CZ, national or subcontinental levels using a weighted average based on harvested area retrieved from the Spatial Production Allocation Model (SPAM) 201044. Details on the GYGA upscaling method can be found in van Bussel et al.13 In the case of top-down approaches, for comparison purposes, it was necessary to aggregate Yp (or Yw) reported for each individual grid into buffers, CZs and countries in order to make them comparable to those reported by GYGA. To do so, Yp (or Yw) from GAEZ and AgMIP was scaled up to buffer, climate zone and country (or subnational levels) considering the crop-specific area within each pixel, as reported by SPAM 201044. For example, for a given buffer, the average Yp (or Yw) was estimated using a weighted average, in which the value of Yp (or Yw) reported for each of the GAEZ or AgMIP grids located within the GYGA buffer was ‘weighted’ according to the SPAM crop-specific area within that grid. The same approach was used to estimate average Yp (or Yw) at the CZ and country (or subcontinental) levels for GAEZ and AgMIP.For a given buffer, CZ or country (or subcontinent), the yield gap was calculated as the difference between Yp (or Yw) and the average farmer yield (actual yield, Ya). The Yp and Yw were taken as the appropriate benchmarks to estimate yield gaps for irrigated and rainfed crops, respectively. To avoid biases due to the source of average actual yield in the estimation of yield gap, we used the average actual yield dataset from GYGA, because it provides estimates of average actual yield disaggregated by water regime for the most recent time period. Actual yield data from GYGA were retrieved from official statistics available at subnational administrative units such as municipalities, counties, departments and subdistrict. The exact number of years of data to calculate average yield is determined by GYGA on a case-by-case basis, following the principle of including as many recent years of data as possible to account for weather variability while avoiding the bias due to a technological time trend and long-term climate change31. Using the GYGA database on average actual yield for estimation of yield gaps does not bias the results from our study, as GYGA favours the use of official sources of average yields at the finer available spatial resolution, which is the same source of actual yield data used by other databases such as FAO and SPAM22,44. In this study, we opted not to use actual yield data from GAEZ, because they derived from FAOSTAT statistics of the years 2000 and 2005, and thus, they could lead to an overestimation of the yield gap in those regions where actual yields have increased over the past two decades19. Finally, extra production potential was calculated based on the yield gap estimated by each approach and the SPAM crop-specific harvested area reported for each buffer, CZ and country (or subcontinent). The top-down and bottom-up approaches were compared in a total of 67 countries, which together account for 74%, 67% and 43% of global maize, rice and wheat harvested areas, respectively (Extended Data Fig. 2). Overall, our comparison included a total of 1,362 buffers located within 870 CZs, with 422 buffers (within 249 CZs) for rainfed maize, 160 buffers (116 CZs) for irrigated maize, 93 buffers (66 CZs) for rainfed rice, 209 buffers (114 CZs) for irrigated rice, 400 buffers (274 CZs) for rainfed wheat and 78 buffers (49 CZs) for irrigated wheat. In all cases, Yp (or Yw), yield gaps and extra production potential were expressed at standard commercial moisture content (that is, 15.5% for maize, 14% for rice and 13.5% for wheat).We assessed the agreement in Yp (or Yw), yield gap, and extra production potential between GYGA and the two databases that follow a top-down approach (GAEZ and AgMIP) separately for each of the spatial levels (buffer, CZ, country or subcontinent) by calculating root-mean-square error (RMSE) and absolute mean error (ME):$${mathrm{RMSE}} = sqrt {frac{{{sum} {(Y_{{mathrm{TD}}} – Y_{{mathrm{BU}}})^2} }}{n}}$$
    (1)
    $${mathrm{ME}} = frac{{{sum} {left( {Y_{{mathrm{TD}}} – Y_{{mathrm{BU}}}} right)} }}{n}$$
    (2)
    where YTD and YBU are the estimated Yp (or Yw), yield gap, or extra production potential for database i following a top-down approach and for GYGA, respectively, and n is the number of paired YTD versus YBU comparisons at a given spatial scale for a given crop in a given country. Separate comparisons were performed for irrigated and rainfed crops.Impact of Yp estimates on food self-sufficiency analysisWe assessed the impact of discrepancies in Yp (or Yw) between top-down and bottom-up approaches on the SSR, which is an important indicator for food security. To do so, we focused on cereal crops in sub-Saharan Africa, and we calculated the SSR for the five main cereal crops in this region (that is, maize, millet, rice, sorghum and wheat) following van Ittersum et al.23. Millet and sorghum were included in the analysis of SSR in sub-Saharan Africa, because together they account for ca. 25% of the total cereal production and ca. 40% of the total cereal harvested area in this region (average over the 2015–2019 period)22. Briefly, we computed current national demand (assumed equal to the 2015 consumption) and the 2015 production of the five cereals to estimate the baseline SSR (that is, in 2015) in ten countries for which Yw (or Yp) data were available in GYGA. Current total cereal demand per country were calculated as the product of current population size derived from United Nations population prospects and cereal demand per capita based on the International Model for Policy Analysis of Agricultural Commodities and Trade (IMPACT)35,45. The annual per-capita demand for the five cereals was expressed in maize yield equivalents by using the crop-specific grain caloric contents, with caloric contents based on FAO food balances46. Current domestic grain production per cereal crop per country (approximately 2015) was calculated as mean actual crop yield (2003–2012) as estimated in GYGA times the 2015 harvested area per crop by FAO22. Total future annual cereal demand per capita (2050), for each of the five cereals and each country, was retrieved from IMPACT modelling results35 using the shared socioeconomic pathway (SSP2, no climate change) from the Intergovernmental Panel on Climate Change fifth assessment47. Total cereal demand per country in 2050 was calculated based on projected 2050 population (medium-fertility variant of United Nations population prospects; https://population.un.org/wpp/) multiplied by the per-capita cereal demand in 2050 from the SSP2 scenario. In our study, we assumed an attainable yield of 80% of Yw for rainfed crops, which is consistent with the original approach followed by van Ittersum et al.23, but, in our study, we also used 80% of Yp for irrigated crops as an estimate of the attainable yield, instead of 85% as in van Ittersum et al.23, to be slightly more conservative. Because the goal was to understand the level of SSR on existing cropland, we assumed no expansion of rainfed or irrigated cropland and no change in net planted area for each of the cereal crops. Our calculations for sub-Saharan Africa may be too pessimistic if genetic progress to increase Yp is achieved. Historically, genetic progress in Yp has contributed to progress in farm yields, although the magnitude of Yp increase is debatable. Progress in elevating Yp of the major cereals would imply, however, that even larger yield gaps need to be overcome than the already large gaps reported herein. Hence, we did not account for changes in genetic Yp in our calculation of SSR by 2050, also because climate change is likely to have a negative effect on Yp and Yw in sub-Saharan Africa.Reporting SummaryFurther information on research design is available in the Nature Research Reporting Summary linked to this article. More

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    Handling of targeted amplicon sequencing data focusing on index hopping and demultiplexing using a nested metabarcoding approach in ecology

    Targeted amplicon sequencing (TAS) or targeted analysis sequencing is a method which addresses the sequencing of specific amplicons and genes. The approach is technologically rooted in next-generation sequencing (NGS), also called high-throughput sequencing (HTS) or massively parallel sequencing and offers the possibility to read millions of sequences in one sequencing run. The rapid evolution of NGS technology with constant increases in sample numbers, data output per sequencing run and associated decreases in costs, has led to this approach becoming widely used in various areas of research. With epigenome, genome and transcriptome sequencing, NGS extends over a wide field, regardless of the different biological disciplines (e.g., botany, ecology, evolutionary biology, genetics, medical sciences, microbiology, zoology, etc.)1,2,3,4,5,6,7,8. In addition to the use of NGS runs in studies to research gene regulation and expression, the characterization of mRNA during transcriptome analyses, the development of molecular markers and genome assembly, another possible application in the context of TAS is the investigation of genetic variation. There is a large range of possible TAS applications including variant detection and tumour profiling in cancer research, the detection of somatic mutations or those associated with susceptibility to disease, new findings in the field of phylogeny and taxonomy studies or the discovery of useful genes for applications in molecular breeding2,3,9,10. In the field of environmental sciences, TAS is becoming increasingly important, as it facilitates the assessment of the taxonomic composition of environmental samples with the help of metabarcoding approaches such as environmental DNA (eDNA) based biomonitoring or food web studies11,12,13.Although NGS-based TAS is a powerful approach, different errors and biases can be introduced in such data sets. Sequencing errors have already been documented in medical studies, wherein factors such as sample handling, polymerase errors and PCR enrichment steps were identified as potential biases14,15. Similarly, other factors such as the variation in sequencing depth between individual samples, sequencing errors rates and index hopping can also play an important role within the analysis of NGS data. The difficulty is that there are currently no general standards requiring detailed reports and explanations to correct such potential errors, and very few studies have addressed this issue. Moreover, there is ever increasing access to NGS platforms, provided by sequencing companies, core facilities and research institutes16,17. NGS services often only provide the sequencing data while general information on the particular NGS run, demultiplexing-efficiency of individual samples and other relevant parameters are usually not passed on. The lack of such information and of a precise description of bioinformatic data processing makes it difficult to assess how the respective NGS run and the subsequent data processing went, which in turn complicates the comparison of results from different studies. Here, we show that specific aspects of library and data preparation have a critical influence on the assignment of sequencing results and how these problems can be addressed using a carabid beetle trophic data set as a case study system.Currently, a widely used approach to study large sample numbers is the analysis of pooled samples, by combining DNA from multiple individuals into one sample of the NGS library, thereby excluding the opportunity of backtracking specific sequences to an individual sample (no individual tagging)18,19,20. In ecological studies (e.g., in biodiversity research and functional ecology), the analysis of such pooled samples may then lead to a decreased estimate of the diversity of the identified species compared to an individual-based analysis21. Aside from the potential loss of information, pooled samples make it impossible to assign a given sample to its specific collection site and thus, the ability to refer to habitat related differences. For individual-level analyses, the ‘nested metabarcoding approach’22 offers a promising solution to problems of complexity and cost. It is both a cost-efficient NGS protocol and one that is scalable to hundreds of individual samples, making it ideal for any study that relies on high sample numbers or that analyses samples which need to be tagged individually, such as in the medical field for patient samples. Using the nested metabarcoding approach, each sample is tagged with four indexes defining a sample. The presence of sequencing errors within the index region can complicate the demultiplexing process and thus the identification of the sample affiliation of individual reads. For a precise assignment of reads to each sample using the index combinations, sequencing errors must be considered in the analysis in order to be able to assign a maximum number of reads.Besides sequencing errors within the different index regions that renders the read assignment difficult, a well-known, but at the same time often ignored problem is ‘index hopping’. This phenomenon, also called index switching/swapping, describes the index mis-assignment between multiplexed libraries and its rate rises as more free adapters or primers are present in the prepared NGS library23,24. Illumina therefore differentiates between combinatorial dual indexing and unique dual indexing. Special kits are offered with unique dual index sequences (set of 96 primer pairs) to counter the problem of index hopping and pitfalls of demultiplexing. This is an option for low sample numbers, as these can still be combined with unique dual indexes (UDIs). If several hundred samples are to be individually tagged in one run, it can be difficult to implement unique dual indexing due to the high number of samples and for cost reasons. Here, the nested metabarcoding approach offers a convenient solution for analysing a large number of individual samples at comparatively low costs. However, it is important to be careful regarding index hopping since more indexes are used in the nested metabarcoding approach than for pooling approaches. For instance, in silico cross-contamination between samples from different studies and altered or falsified results can occur if a flow cell lane is shared and the reads were incorrectly assigned. Even where samples are run exclusively on a single flow cell, index hopping may result in barcode switching events between samples that lead to mis-assignment of reads.For library preparations of Illumina NGS runs, two indexes are usually used to tag the individual samples (dual indexing)25. Illumina offers the option to do the demultiplexing and convert the sequenced data into FASTQ file formats using the supplied ‘bcl2fastq’ or ‘bcl2fastq2’ conversion software tool26. This demultiplexing is a crucial step, as it is here that the generated DNA sequences are assigned to the samples. In most cases, the data is already provided demultiplexed after the NGS run by the sequencing facility, especially if runs were shared between different studies/sample sets. Researchers starting the bioinformatic analysis with demultiplexed data assume that the assignment of the sequences to samples was correct. Verifying this is extremely difficult because the provided data sets lack all the information on the demultiplexing settings and, above all, on the extent of sequencing errors within indexes and index hopping. As a consequence, sequences can be incorrectly assigned to samples and, in case of a shared flow cell, even across sample sets. These steps of bioinformatic analysis are very often outsourced to companies and details on demultiplexing are seldom reported, showing that the problem of read mis-assignment has received little attention so far. However, it is known that demultiplexing errors occur and depend on various factors such as the Illumina sequencing platform, the library type used and index combinations23,24,25,27,28,29,30. The few existing studies investigating index hopping in more detail give rates of 0.2–10%24,31,32,33,34. This indicates the importance of being able to estimate the extent of index hopping for a specific library. The problem of sequencing errors within indexes and index hopping can become particularly significant if, due to the large number of individual samples, libraries were constructed with two instead of one index pair, such as it is the case in the nested metabarcoding approach35. Then, one is inevitably confronted with the effect of sequencing errors and index hopping on demultiplexing and subsequently on the data output.After each NGS run, the combination of computational power and background knowledge in bioinformatics are needed to ensure time-efficient and successful data analysis36. But even for natural scientists with considerable bioinformatic experience, there is a lack of know-how or even rules-of-thumb in this still nascent field. It is well known that specific decisions have a marked impact on the outcome of a study, with both the sequencing platform and software tools significantly affecting the results and thereby the interpretation of the sequencing information37. Knowledge of the individual data processing steps, such as for the demultiplexing, is also often missing or poorly described. Information on how to minimize data loss within the individual steps for data preparation of the NGS data is also mostly not explained. Given this lack of detail, it is a challenge to understand what was done during sample processing and data analysis, and impossible to compare the outcomes of different studies. To date, published NGS studies, such as TAS or DNA metabarcoding studies, are difficult to compare or evaluate because of the lack of this essential information on data processing. This is particularly important as NGS is increasingly being done by external service providers. As a consequence, there is a pressing need for comprehensive protocols that detail the aspects that need to be considered during analysis.Using a case study on the dietary choice of carabid beetles (Coleoptera: Carabidae) in arable land, we detail a comprehensive protocol that describes an entire workflow targeting ITS2 fragments, using an Illumina HiSeq 2500 system and applying the nested metabarcoding approach22 to identify those species of weed seeds consumed by carabid individuals. We demonstrate a concept that employs bioinformatic tools for targeted amplicon sequencing in a defined order. By analysing the effects of sequencing errors and index hopping on demultiplexing and data trimming, we show the importance of describing the software and pipeline used and its version, as well as specifying software configurations and thresholds settings for each TAS data set to receive a realistic data output per sample. Without this information, there is the possibility of incorrectly assigning samples or not receiving the maximum or at least a sufficient number of sequences which in turn would hamper the results.The concept described below can be used to analyse a large number of samples, here to identify food items on species-specific level, and to address the possible problems that may arise in NGS data processing. We identify problems to overcome and potential solutions by examining: (i) the variation in sequencing depth of individually tagged samples and the effect of library preparation on the data output; (ii) the influence of sequencing errors within index regions and its consequences for demultiplexing; and, (iii) the effect of index hopping. By doing this, we highlight the benefits of a detailed protocol for bioinformatic analysis of a given data set, and the importance of the reporting of bioinformatic parameters, especially for the demultiplexing, and thresholds to be used for meaningful data interpretation. More