Ecology

Parasites have frequently been observed on the gills of coleoid cephalopods during ROV dives in the mesopelagic waters of the Monterey Submarine Canyon. Here, we demonstrate that at least two parasite species can be distinguished from ROV-collected specimens. Based on morphology, the first parasite was identified as the protist Hochbergia cf. moroteuthensis. Although the original description of H. moroteuthensis struggled to assign a taxonomic rank, the authors noted that the presence of trichocysts and an apical pore bear similarities to those of dinoflagellates in an encysted life stage29,30. Using Sanger sequencing and dinoflagellate cyst-specific primers, we confirm this parasite to be a dinoflagellate that forms a sister group to members of the Oodinium genus. The second parasite could not be matched to any documented morphological descriptions, and DNA barcoding was only able to resolve a short sequence that does not provide for a reliable identification.Hochbergia moroteuthensis appears to be a common parasite of midwater cephalopods and has previously been collected off the gills of twenty cephalopod species29,30. These include five taxa investigated here (C. calyx, V. infernalis, Galiteuthis spp., Gonatus spp. and Japetella diaphana), with Taonius sp. new to the list. While H. cf. moroteuthensis found in this study was somewhat smaller than the type series (0.5–1.4 mm versus 1.19–1.99)30, it was within the range of those reported by McLean et al.29 on the squids Stigmatoteuthis dofleini Pfeffer, 1912 and Abralia trigonura Berry, 1913 (i.e. 0.56 to 1.10 mm on average in length)29. The latter authors noticed that parasite size, color (i.e. white to yellow) and thecal plate morphology may differ between host species, which could indicate multiple Hochbergia species. It should, however, be noted that it is unknown whether H. moroteuthensis maximum growth is dependent on host size or whether the investigated parasites were simply in different growth stages given the study’s relatively small samples sizes. Although we did not compare H. cf. moroteuthensis morphology across hosts in great detail, the partial 18S rRNA sequences obtained for parasites on Gonatus berryi and Chiroteuthis calyx were identical. Further research is therefore warranted to investigate species-specific parasite differences and speciation among hosts.The genetic relatedness between H. cf. moroteuthensis and its Oodinium sister group is further supported by several morphological features. First, the lack of distinct dinoflagellate characters, ovoid shape and the presence of trichocysts, have also been noted for Oodinium cysts41,42,43. McLean et al.29 further reported that the nucleus of the single-celled H. moroteuthensis cyst contains diffuse chromatin, a feature unlike most dinoflagellates that possess well-defined rod-like chromosomes42. Remarkably, dinoflagellates within Oodinium are known to alternate between both non-dinokaryotic and dinokaryotic nuclei within their life cycles, which could explain H. moroteuthensis’ diffuse chromatin42,43. Similarities between H. moroteuthensis and Oodinium further extend to the parasitic life style with primarily pelagic hosts. Dinoflagellates in the Oodinium genus are all known to be ectoparasitic, infecting ctenophores, chaetognaths, annelids, larvaceans and a hydromedusa41,43,44,45,46.In spite of these similarities, there are also several noteworthy morphological differences between H. moroteuthensis and members of the Oodinium genus. Young Oodinium cysts generally have a white to yellow coloring, with older cysts taking a yellow–brown or dark brown tint41,43,44. Oodinium cysts also possess relatively simple thecal plates and above all, have a distinct peduncle, or stalk, with which they attach to the host and which is thought to serve as feeding apparatus41,43,47. Maximum lengths for Oodinium cysts have been reported up to 0.39 mm43,46. In contrast, cysts in H. moroteuthensis possess a white to yellow coloring, an intricate pattern of triangular plates, reach sizes up to 1.99 mm long, and have a simple holdfast area with an oval aperture that likely anchors them to the host30. Currently, both Oodinium and Hochbergia form a genetically distinct clade within the Dinophyceae and analysis of further specimens and genetic markers might provide more insight into their relatedness and specialization on primarily pelagic hosts. Additionally, analysis of fast- and slow-evolving genetic markers might resolve the polytomy observed in the phylogenetic trees, which were also present in the phylogenetic reconstruction of the DINOREF reference database by Mordret et al.32.The genetic similarity of H. cf. moroteuthensis to an unidentified eukaryote from the water column and the fact that we encountered the protozoans in an encysted stage, strongly suggests that these dinoflagellates infect their cephalopod hosts through a free-living life stage. Many parasitic dinoflagellates, including Oodinium, alternate between a motile free-living stage—the dinospore—that forms a vegetative feeding stage—the trophont—upon attachment to the host41,47,48. During this vegetative stage, the trophont grows greatly in size but without cellular division. Once mature, the trophont detaches from the host to divide into multiple flagellated dinospores. The dinospores disperse into the water column, free to infect new hosts (Fig. 6)41,47,48.Figure 6Theorized life cycle of Hochbergia moroteuthensis. (a) The vegetative trophont (feeding life stage) grows without cellular division on the cephalopod’s gills. (b) The mature trophont detaches and (c) divides into motile dinospores, (d) free to infect new hosts in the water column. Illustration (b) trophont adapted from Shinn & McLean30.Full size imageSuch a free-living life stage is consistent with H. moroteuthensis’ wide geographic distribution. Free-living dinospores are easily dispersed by ocean currents, and observations in both the North Pacific Ocean and the Gulf of Mexico could indicate large-scale ocean connectivity, potentially beyond the distribution reported here29. This dispersal may also offer H. moroteuthensis a wide range of infection possibilities and explain why trophonts are found in twenty-one different cephalopod taxa. Nevertheless, population genetic structure needs to be investigated, as it is currently unknown if the parasites represent multiple species.Free-living dinospores might also explain H. moroteuthensis’ location on the exterior gill tissue. With dinospores free in the water column, the fastest pathway to a cephalopod’s interior is through ‘inhalation’. In this process, cephalopods actively force water through their gills, making these the first organs Hochbergia would encounter. Respiratory organs give direct access to the cephalopod’s blood stream, and therefore offer a suitable environment (i.e. nutrient and oxygen rich) for development into a trophont. Gills also provide interstices that could simply trap dinospores. Either way, there was only one occasion (i.e. out of 355) where trophonts were seen on other body parts besides the gills (Fig. 4e). In comparison, several Oodinium parasites are also known to attach to specific host-body parts, apparently preferring sites involved in locomotor movement. For instance, Oodinium jordani McLean & Nielsen, 1989 is known to attach to the fin of the chaetognath Sagitta elegans Verrill, 187346, while O. pouchetti is mostly found on the tail of appendicularians41, and Oodinium sp. collected off various ctenophores appears to prefer attachment close to or within the beating comb rows44. Whether these surface areas offer highest encounter rates or provide a physical benefit such as enhanced oxygenation remains unknown.The increased prevalence of H. cf. moroteuthensis observed in the most abundant cephalopod, Chiroteuthis, and in the other adult cephalopods is in line with infection dynamics known from other wildlife parasites, where the probability of a parasitic infection increases with host density and age49,50,51. Following this, dinospores in the Monterey Submarine Canyon have more opportunities to encounter common squids like Chiroteuthis52 and longer-lived cephalopods. Alternatively, it is possible that the increased parasite load in adults is simply the result of larger gill surface areas when compared to juveniles. However, when comparing prevalence between host species, it should be noted that the maximum adult sizes for C. calyx (up to 100 mm in mantle length, ML) are smaller than those of Galiteuthis (500 mm ML), Taonius (660 mm ML) and Japetella (144 mm ML) among specimens found in the Monterey Submarine Canyon53,54.Other factors that might explain the observed prevalence include parasite preferences for host physiology (e.g. respiration rates) or confinement to a certain depth range18. Although Chiroteuthis, Galiteuthis, Taonius and Japetella partially overlap in their depth distributions, Chiroteuthis generally remains above the core of the oxygen minimum zone, located around 700 m in Monterey Bay52,55. Galiteuthis, on the other hand, has a bimodal distribution, with older individuals known to migrate below the oxygen minimum core52,55,56. If dinospore viability is restricted to more shallow depths, the probability of infection for Galiteuthis could decrease when living at deeper depths. This is further supported by Taonius, which showed a comparable bimodal distribution to Galiteuthis52 and shared a similar parasite prevalence. Furthermore, Japetella is the deepest living cephalopod investigated and harbored relatively few Hochbergia trophonts. In spite of this, it is unknown how long it takes for H. moroteuthensis dinospores to develop into mature trophonts and over what time frames they may accumulate on their hosts. Lab-based experiments with Oodinium sp. on the ctenophore Beroe abyssicola Mortensen, 1927 showed that trophonts needed approximately 20 days to grow from 35 µm in length to their mature size of 350 µm at 10 °C44. Given that H. moroteuthensis can grow over five times larger and lives at colder temperatures depending on its host distribution, growth periods may be substantially longer.When looking at the prevalence of H. cf. moroteuthensis over time, only Taonius appeared to be showing an increase in infected individuals over the years. Present results, however, are insufficient to determine whether this increase is the result of environmental change or part of natural variability. We therefore recommend continued monitoring to determine long term trends. Based on the monthly prevalence, it is likely that Chiroteuthis acts as a reservoir for Hochbergia parasites throughout the year. Galiteuthis, Japetella and Taonius show more seasonal dynamics. It may be that the reported seasonality is related to upwelling events or environmental cues promoting dinospore formation (e.g. increasing temperatures)50. Alternatively, cephalopods might be more susceptible to infections in certain months, or have higher resistance in others. Taonius, for example, had a markedly lower parasite load on average than Galiteuthis despite similar prevalence estimates (Tables 1 and 2), potentially indicating some sort of resistance mechanism. More research is warranted to confirm any host resistance and the influence of depth or seasonal effects.The other parasite type found in ROV-collected specimens of Vampyroteuthis infernalis and Gonatus spp. needs further characterization. Although DNA barcoding was able to resolve a short sequence that potentially places it within the phylum Apicomplexa, it appears more likely that this genetic material originated from contamination with a different parasite. Apicomplexa reported in cephalopods generally infect the digestive tract and are morphologically different from the parasites observed here19.In conclusion, our findings highlight the need for further investigation of cephalopods and their gill parasites. Considering that parasites influence biodiversity and that cephalopods form key links in pelagic food webs, future research should be focused at assessing potential effects on cephalopod physiology. For example, if H. moroteuthensis limits longevity or reproduction in common squids like C. calyx, then changes in parasite abundance might result in cascading effects on abundance of Chiroteuthis’ prey, predators and competitors. Additionally, baseline estimates of parasite prevalence are crucial to fully understand whether midwater host-parasite systems are at risk from increasing anthropogenic stressors and how they will change over time. While ROV observations have proven key to estimate prevalence and infection intensity here, trawled specimens continue to be valuable for verification of parasite species and obtaining material for genetic analyses, even if slightly damaged. We therefore recommend combining ROV observations with periodic trawling in future studies, since ROVs may not reveal smaller parasites, early infections or parasites in animals with tissue that is not transparent. More

Australia’s tropical rainforests are some of the oldest in the world.Credit: Alexander Schenkin

The rate of tree dying in the old-growth tropical forests of northern Australia each year has doubled since the 1980s, and researchers say climate change is probably to blame.The findings, published today in Nature1, come from an extraordinary record of tree deaths catalogued at 24 sites in the tropical forests of northern Queensland over the past 49 years.“Trees are such long-living organisms that it really requires huge amounts of data to be able to detect changes in such rare events as the death of a tree,” says lead author David Bauman, a plant ecologist at the University of Oxford, UK. The sites were initially surveyed every two years, then every three to four years, he explains, and the analysis focused on 81 key species.Bauman and his team recorded that 2,305 of these trees have died since 1971. But they calculated that, from the mid-1980s, tree mortality risk increased from an average of 1% a year to 2% a year (See ‘Increasing death rate’).

Bauman says that trees help to slow global warming because they absorb carbon dioxide, so an increase in tree deaths reduces forests’ carbon-capturing ability. “Tropical forests are critical to climate change, but they’re also very vulnerable to it,” he explains.Climate changeThe study found that the rise in death rate occurred at the same time as a long-term trend of increases in the atmospheric vapour pressure deficit, which is the difference between the amount of water vapour that the atmosphere can hold and the amount of water it does hold at a given time. The higher the deficit, the more water trees lose through their leaves. “If the evaporative demand at the leaf level can’t be matched by water absorption in fine roots, it can lead to leaves wilting, whole branches dying and, if the stress is sustained, to tree death,” Bauman says.The researchers looked at other climate-related trends — including rising temperatures and an estimate of drought stress in soils — but they found that the drying atmosphere had the strongest effect. “What we show is that this increase [in tree mortality risk] also closely followed the increase in atmospheric water stress, or the drying power of air, which is a consequence of the temperature increase due to climate change,” Bauman explains.Of the 81 tree species that the team studied, 70% showed an increase in mortality risk over the study period, including the Moreton Bay chestnut (Castanospermum australe), white aspen (Medicosma fareana) and satin sycamore (Ceratopetalum succirubrum).The authors also saw differences in mortality in the same tree species across plots, depending on how high the atmospheric vapour pressure deficit was in each plot.“This is one data set where the trees have been monitored in reasonably good detail since the early ’70s, and this is a really top-notch analysis of it,” says Belinda Medlyn, an ecosystem scientist at University of Western Sydney, Australia.But she says that more experiments are needed to determine whether the vapour pressure deficit is the biggest climate-related contributor to the increase in tree deaths. More

Young cerebrospinal fluid probably improves the conductivity of the neurons in ageing mice.Credit: Qilai Shen/Bloomberg/Getty

Young brain fluid improves memory in old miceCerebrospinal fluid (CSF) from young mice can improve memory function in older mice, researchers report in Nature (T. Iram et al. Nature 605, 509–515; 2022).A direct brain infusion of young CSF probably improves the conductivity of the neurons in ageing mice, which improves the process of making and recalling memories.CSF is a cocktail of essential ions and nutrients that cushions the brain and spinal cord and is essential for normal brain development. But as mammals age, CSF loses some of its punch. Those changes might affect cells related to memory, says co-author Tal Iram, a neuroscientist at Stanford University in California.The researchers found that young CSF helps ageing mice to generate more early-stage oligodendrocytes, cells in the brain that produce the insulating sheath around nerve projections and help to maintain brain function.The team suggest that the improvements are largely due to a specific protein in the fluid.“This is super exciting from the perspective of basic science, but also looking towards therapeutic applications,” says Maria Lehtinen, a neurobiologist at Boston Children’s Hospital in Massachusetts.Gender bias worms its way into parasite namingA study examining the names of nearly 3,000 species of parasitic worm discovered in the past 20 years reveals a markedly higher proportion named after male scientists than after female scientists — and a growing appetite for immortalizing friends and family members in scientific names.Robert Poulin, an ecological parasitologist at the University of Otago in Dunedin, New Zealand, and his colleagues combed through papers published between 2000 and 2020 that describe roughly 2,900 new species of parasitic worm (R. Poulin et al. Proc. R. Soc. B https://doi.org/htqn; 2022). The team found that well over 1,500 species were named after their host organism, where they were found or a prominent feature of their anatomy.

Source: R. Poulin et al. Proc. R. Soc. B https://doi.org/htqn (2022)

Many others were named after people, ranging from technical assistants to prominent politicians. But just 19% of the 596 species named after eminent scientists were named after women, a percentage that barely changed over the decades (see ‘Parasite name game’). Poulin and his colleagues also noticed an upward trend in the number of parasites named after friends, family members and even pets of the scientists who formally described them. This practice should be discouraged, Poulin argues.

Sea anemones turn oxybenzone into a light-activated agent that can bleach and kill corals.Credit: Georgette Douwma/Getty

Anemones suggest why sunscreen turns toxic in seaA common but controversial sunscreen ingredient that is thought to harm corals might do so because of a chemical reaction that causes it to damage cells in the presence of ultraviolet light.Researchers have discovered that sea anemones, which are similar to corals, make the sun-blocking molecule oxybenzone water-soluble by tacking a sugar onto it. This inadvertently turns oxybenzone into a molecule that — instead of blocking UV light — is activated by sunlight to produce free radicals that can bleach and kill corals. The animals “convert a sunscreen into something that’s essentially the opposite of a sunscreen”, says Djordje Vuckovic, an environmental engineer at Stanford University in California.It’s not clear how closely these laboratory-based studies mimic the reality of reef ecosystems. The concentration of oxybenzone at a coral reef can vary widely, depending on factors such as tourist activity and water conditions. And other factors threaten the health of coral reefs; these include climate change, ocean acidification, coastal pollution and overfishing. The study, published on 5 May (D. Vuckovic et al. Science 376, 644–648; 2022) does not show where oxybenzone ranks in the list. More

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain
the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in
Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles
and JavaScript. More

Dargie, G. C. et al. Age, extent and carbon storage of the central Congo Basin peatland complex. Nature 542, 86–90 (2017). This study describes the large extent and huge carbon stocks of the Congo Basin peatlands.Article 

Google Scholar 
Page, S. E., Rieley, J. O. & Banks, C. J. Global and regional importance of the tropical peatland carbon pool. Glob. Change Biol. 17, 798–818 (2011). This is a comprehensive assessment of the extent, volume and carbon stocks of peatlands across the tropics, highlighting their importance in the global carbon cycle and key uncertainties.Article 

Google Scholar 
Yu, Z., Loisel, J., Brosseau, D. P., Beilman, D. W. & Hunt, S. J. Global peatland dynamics since the Last Glacial Maximum. Geophys. Res. Lett. 37, L13402 (2010).
Google Scholar 
Gumbricht, T. et al. An expert system model for mapping tropical wetlands and peatlands reveals South America as the largest contributor. Glob. Change Biol. 23, 3581–3599 (2017).Article 

Google Scholar 
Olsson, L. et al. Climate change and land (eds Shukla, P. R. et al.) 345–436 (IPCC, 2019).Leifeld, J. & Menichetti, L. The underappreciated potential of peatlands in global climate change mitigation strategies. Nat. Commun. 9, 1071 (2018).Article 

Google Scholar 
Smith, P. et al. Climate change 2014: mitigation of climate change. Contribution of Working Group III to the fifth assessment report of the Intergovernmental Panel on Climate Change (eds Edenhofer, O. et al.) 811–922 (Cambridge Univ. Press, 2014).Goldstein, A. et al. Protecting irrecoverable carbon in Earth’s ecosystems. Nat. Clim. Chang. 10, 287–295 (2020). This study evaluates ecosystems on the basis of the size of carbon stocks that are vulnerable to release upon land-use conversion and not recoverable on timescales relevant to avoiding dangerous climate impacts; it emphasizes the high density of irrecoverable carbon in tropical peatlands.Article 

Google Scholar 
Griscom, B. W. et al. Natural climate solutions. Proc. Natl. Acad. Sci. USA 114, 11645–11650 (2017).Article 

Google Scholar 
Leifeld, J., Wüst-Galley, C. & Page, S. Intact and managed peatland soils as a source and sink of GHGs from 1850 to 2100. Nat. Clim. Chang. 9, 945–947 (2019).Article 

Google Scholar 
Intergovernmental Panel on Climate Change. Climate change and land (IPCC, 2019).Pan, Y. et al. A large and persistent carbon sink in the world’s forests. Science 333, 988–993 (2011).Article 

Google Scholar 
Page, S., Wüst, R. & Banks, C. Past and present carbon accumulation and loss in Southeast Asian peatlands. PAGES News 18, 25–27 (2010).Article 

Google Scholar 
Page, S. E. et al. A record of Late Pleistocene and Holocene carbon accumulation and climate change from an equatorial peat bog (Kalimantan, Indonesia): implications for past, present and future carbon dynamics. J. Quat. Sci. 19, 625–635 (2004).Article 

Google Scholar 
Dommain, R., Couwenberg, J. & Joosten, H. Development and carbon sequestration of tropical peat domes in south-east Asia: links to post-glacial sea-level changes and Holocene climate variability. Quat. Sci. Rev. 30, 999–1010 (2011). This is a comprehensive assessment of peatland development in Southeast Asia, exploring regional differences in rates of peat formation and carbon accumulation.Article 

Google Scholar 
Ruwaimana, M., Anshari, G. Z., Silva, L. C. R. & Gavin, D. G. The oldest extant tropical peatland in the world: a major carbon reservoir for at least 47,000 years. Environ. Res. Lett. 15, 114027 (2020). This study compares the development of coastal and inland peatlands in West Kalimantan, Indonesia, and provides a description of the oldest known peat deposit in Southeast Asia.Article 

Google Scholar 
Anshari, G., Kershaw, A. P., Kaars, S. V. D. & Jacobsen, G. Environmental change and peatland forest dynamics in the Lake Sentarum area, West Kalimantan, Indonesia. J. Quat. Sci. 19, 637–655 (2004).Article 

Google Scholar 
Dommain, R., Couwenberg, J. & Joosten, H. Hydrological self-regulation of domed peatlands in south-east Asia and consequences for conservation and restoration Mires Peat 6, 1–17 2010).
Google Scholar 
Jones, M. B. & Muthuri, F. M. Standing biomass and carbon distribution in a papyrus (Cyperus papyrus L.) swamp on Lake Naivasha, Kenya. J. Trop. Ecol. 13, 347–356 (1997).Article 

Google Scholar 
Saunders, M. J., Jones, M. B. & Kansiime, F. Carbon and water cycles in tropical papyrus wetlands. Wetl. Ecol. Manag. 15, 489–498 (2007).Article 

Google Scholar 
Burrough, S. L., Thomas, D. S. G., Orijemie, E. A. & Willis, K. J. Landscape sensitivity and ecological change in western Zambia: the long-term perspective from dambo cut-and-fill sediments. J. Quat. Sci. 30, 44–58 (2015).Article 

Google Scholar 
Davenport, I. J. et al. First evidence of peat domes in the Congo Basin using LiDAR from a fixed-wing drone. Remote Sens. 12, 2196 (2020).Article 

Google Scholar 
Alsdorf, D. et al. Opportunities for hydrologic research in the Congo Basin. Rev. Geophys. 54, 378–409 (2016).Article 

Google Scholar 
Biddulph, G. E. et al. Current knowledge on the Cuvette Centrale peatland complex and future research directions. Bois For. Trop. 350, 3–14 (2021).Article 

Google Scholar 
Lähteenoja, O. et al. The large Amazonian peatland carbon sink in the subsiding Pastaza–Marañón foreland basin, Peru. Glob. Change Biol. 18, 164–178 (2012).Article 

Google Scholar 
Kelly, T. J. et al. The vegetation history of an Amazonian domed peatland. Palaeogeogr. Palaeoclimatol. Palaeoecol. 468, 129–141 (2017).Article 

Google Scholar 
Draper, F. C. et al. The distribution and amount of carbon in the largest peatland complex in Amazonia. Environ. Res. Lett. 9, 124017 (2014). Using a combination of remote sensing and field data, this study provides an assessment of the distribution of above- and belowground peatland carbon stocks in the Pastaza–Marañon foreland basin in Peruvian Amazonia.Article 

Google Scholar 
Phillips, S., Rouse, G. E. & Bustin, R. M. Vegetation zones and diagnostic pollen profiles of a coastal peat swamp, Bocas del Toro, Panamá. Palaeogeogr. Palaeoclimatol. Palaeoecol. 128, 301–338 (1997).Article 

Google Scholar 
Sjögersten, S. et al. Coastal wetland ecosystems deliver large carbon stocks in tropical Mexico. Geoderma 403, 115173 (2021).Article 

Google Scholar 
Joosten, H. in Tropical Peatland Ecosystems (eds Osaki, M. & Tsuji, N.) 33–48 (Springer, 2016).Anderson, J. A. R. in Mires: Swamp, Bog, Fen and Moor: Regional Studies (ed. Gore, A. J. P.) 191–199 (Elsevier, 1983).Draper, F. C. et al. Peatland forests are the least diverse tree communities documented in Amazonia, but contribute to high regional beta-diversity. Ecography 41, 1256–1269 (2018).Article 

Google Scholar 
Anderson, J. A. R. Ecology and Forest Types of The Peat Swamp Forests of Sarawak and Brunei in Relation to their Silviculture. Thesis, Univ. Edinburgh (1961).Freund, C. A., Harsanto, F. A., Purwanto, A., Takahashi, H. & Harrison, M. E. Microtopographic specialization and flexibility in tropical peat swamp forest tree species. Biotropica 50, 208–214 (2018).Article 

Google Scholar 
Lampela, M. et al. Ground surface microtopography and vegetation patterns in a tropical peat swamp forest. CATENA 139, 127–136 (2016).Article 

Google Scholar 
Miyamoto, K. et al. Habitat differentiation among tree species with small-scale variation of humus depth and topography in a tropical heath forest of Central Kalimantan, Indonesia. J. Trop. Ecol. 19, 43–54 (2003).Article 

Google Scholar 
Miettinen, J., Shi, C. & Liew, S. C. Land cover distribution in the peatlands of peninsular Malaysia, Sumatra and Borneo in 2015 with changes since 1990. Glob. Ecol. Conserv. 6, 67–78 (2016).Article 

Google Scholar 
Wijedasa, L. S. et al. Carbon emissions from South-East Asian peatlands will increase despite emission-reduction schemes. Glob. Change Biol. 24, 4598–4613 (2018).Article 

Google Scholar 
Page, S. E. & Hooijer, A. In the line of fire: the peatlands of Southeast Asia. Phil. Trans. R. Soc. B 371, 20150176.(2016).Article 

Google Scholar 
Hergoualc’h, K., Gutiérrez-Vélez, V. H., Menton, M. & Verchot, L. V. Characterizing degradation of palm swamp peatlands from space and on the ground: an exploratory study in the Peruvian Amazon. For. Ecol. Manag. 393, 63–73 (2017).Article 

Google Scholar 
Horn, C. M., Vargas Paredes, V. H., Gilmore, M. P. & Endress, B. A. Spatio-temporal patterns of Mauritia flexuosa fruit extraction in the Peruvian Amazon: implications for conservation and sustainability. Appl. Geogr. 97, 98–108 (2018).Article 

Google Scholar 
Dargie, G. C. et al. Congo Basin peatlands: threats and conservation priorities. Mitig. Adapt. Strateg. Glob. Change 24, 669–686 (2019).Article 

Google Scholar 
Grundling, P.-L. & Grootjans, A. P. in The Wetland Book. II: Distribution, Description, and Conservation (eds Finlayson, M., Milton, G., Prentice, R. & Davidson, N.) (Springer, 2018).Roucoux, K. H. et al. Threats to intact tropical peatlands and opportunities for their conservation. Conserv. Biol. 31, 1283–1292 (2017).Article 

Google Scholar 
Baird, A. J. et al. High permeability explains the vulnerability of the carbon store in drained tropical peatlands. Geophys. Res. Lett. 44, 1333–1339 (2017). This study finds that the permeability of ombrotrophic tropical peat is higher than expected, resulting in deep water tables in ditched tropical peatlands and associated high rates of peat oxidation.Article 

Google Scholar 
Kelly, T. J. et al. The high hydraulic conductivity of three wooded tropical peat swamps in northeast Peru: measurements and implications for hydrological function. Hydrol. Process. 28, 3373–3387 (2014).Article 

Google Scholar 
Tonks, A. J. et al. Impacts of conversion of tropical peat swamp forest to oil palm plantation on peat organic chemistry, physical properties and carbon stocks. Geoderma 289, 36–45 (2017).Article 

Google Scholar 
Mezbahuddin, M., Grant, R. F. & Hirano, T. How hydrology determines seasonal and interannual variations in water table depth, surface energy exchange, and water stress in a tropical peatland: modeling versus measurements. J. Geophys. Res. Biogeosci. 120, 2132–2157 (2015).Article 

Google Scholar 
Laurén, A. et al. Nutrient balance as a tool for maintaining yield and mitigating environmental impacts of Acacia plantation in drained tropical peatland — description of plantation simulator. Forests 12, 312 (2021).Article 

Google Scholar 
Hooijer, A. et al. Subsidence and carbon loss in drained tropical peatlands. Biogeosciences 9, 1053–1071 (2012).Article 

Google Scholar 
Anshari, G. Z., Gusmayanti, E. & Novita, N. The use of subsidence to estimate carbon loss from deforested and drained tropical peatlands in Indonesia. Forests 12, 732 (2021).Article 

Google Scholar 
Evans, C. D. et al. A novel low-cost, high-resolution camera system for measuring peat subsidence and water table dynamics. Front. Environ. Sci. 9, 33 (2021).
Google Scholar 
Evans, C. D. et al. Rates and spatial variability of peat subsidence in Acacia plantation and forest landscapes in Sumatra, Indonesia. Geoderma 338, 410–421 (2019).Article 

Google Scholar 
Hoyt, A. M., Chaussard, E., Seppalainen, S. S. & Harvey, C. F. Widespread subsidence and carbon emissions across Southeast Asian peatlands. Nat. Geosci. 13, 435–440 (2020). Using remote sensing, this study quantifies the rate of peat subsidence and carbon loss across peatlands in Southeast Asia.Article 

Google Scholar 
Cobb, A. R., Dommain, R., Tan, F., Heng, N. H. E. & Harvey, C. F. Carbon storage capacity of tropical peatlands in natural and artificial drainage networks. Environ. Res. Lett. 15, 114009 (2020).Article 

Google Scholar 
Ritzema, H., Limin, S., Kusin, K., Jauhiainen, J. & Wösten, H. Canal blocking strategies for hydrological restoration of degraded tropical peatlands in central Kalimantan, Indonesia. CATENA 114, 11–20 (2014).Article 

Google Scholar 
Hooijer, A., Vernimmen, R., Visser, M. & Mawdsley, N. Flooding projections from elevation and subsidence models for oil palm plantations in the Rajang Delta peatlands, Sarawak, Malaysia (Deltares, 2015).Sumarga, E., Hein, L., Hooijer, A. & Vernimmen, R. Hydrological and economic effects of oil palm cultivation in Indonesian peatlands. Ecol. Soc. 21, 52 (2016).Article 

Google Scholar 
Evers, S., Yule, C. M., Padfield, R., O’Reilly, P. & Varkkey, H. Keep wetlands wet: the myth of sustainable development of tropical peatlands — implications for policies and management. Glob. Change Biol. 23, 534–549 (2017). This study reviews the ecosystem services provided by Southeast Asian peatlands and discusses key policy challenges for peatland management.Article 

Google Scholar 
Tan, Z. D., Lupascu, M. & Wijedasa, L. S. Paludiculture as a sustainable land use alternative for tropical peatlands: a review. Sci. Total Environ. 753, 142111 (2021). This study evaluates the current understanding of and opportunities for paludiculture in the context of tropical peatlands, emphasizing that tropical paludiculture will be heavily influenced by socioeconomic considerations.Article 

Google Scholar 
Haraguchi, A. in Tropical Peatland Ecosystems (Osaki, M. & Tsuji, N.) 297–311 (Springer, 2016).Wösten, J. H. M., Ismail, A. B. & van Wijk, A. L. M. Peat subsidence and its practical implications: a case study in Malaysia. Geoderma 78, 25–36 (1997).Article 

Google Scholar 
Grealish, G. J. & Fitzpatrick, R. W. Acid sulphate soil characterization in Negara Brunei Darussalam: a case study to inform management decisions. Soil. Use Manag. 29, 432–444 (2013).Article 

Google Scholar 
Klepper, O., Chairuddin, G. T., Iriansyah & Rijksen, H. D. Water quality and the distribution of some fishes in an area of acid sulphate soils, Kalimantan, Indonesia. Hydrobiol. Bull. 25, 217–224 (1992).Article 

Google Scholar 
Shamshuddin, J. & Muhrizal, S. Chemical pollution in acid sulfate soils. Proc. Geol. Soc. Malaysia Annu. Geol.Conf. 2000, 231–234 (2000).
Google Scholar 
Suwardi. Utilization and improvement of marginal soils for agricultural development in Indonesia. IOP Conf. Ser. Earth Environ. Sci. 383, 012047 (2019).Article 

Google Scholar 
Hirano, T., Jauhiainen, J., Inoue, T. & Takahashi, H. Controls on the carbon balance of tropical peatlands. Ecosystems 12, 873–887 (2009).Article 

Google Scholar 
Stumm, W. & Morgan, J. J. Aquatic Chemistry: Chemical Equilibria and Rates in Natural Waters (Wiley, 1996).Billett, M. F., Garnett, M. H. & Dinsmore, K. J. Should aquatic CO evasion be included in contemporary carbon budgets for peatland ecosystems? Ecosystems 18, 471–480 (2015).Article 

Google Scholar 
Chimner, R. A. & Ewel, K. C. A tropical freshwater wetland: II. Production, decomposition, and peat formation. Wetl. Ecol. Manag. 13, 671–684 (2005).Article 

Google Scholar 
Hoyos-Santillan, J. et al. Getting to the root of the problem: litter decomposition and peat formation in lowland neotropical peatlands. Biogeochemistry 126, 115–129 (2015).Article 

Google Scholar 
Könönen, M. et al. Land use increases the recalcitrance of tropical peat. Wetl. Ecol. Manag. 24, 717–731 (2016).Article 

Google Scholar 
Sangok, F. E., Maie, N., Melling, L. & Watanabe, A. Evaluation on the decomposability of tropical forest peat soils after conversion to an oil palm plantation. Sci. Total Environ. 587–588, 381–388 (2017).Article 

Google Scholar 
Yule, C. M., Lim, Y. Y. & Lim, T. Y. Degradation of tropical Malaysian peatlands decreases levels of phenolics in soil and in leaves of Macaranga pruinosa. Front. Earth Sci. 4, 1–9 (2016).Article 

Google Scholar 
Yu, Z. et al. Peatlands and their role in the global carbon cycle. Eos 92, 97–98 (2011).Article 

Google Scholar 
Lähteenoja, O., Ruokolainen, K., Schulman, L. & Oinonen, M. Amazonian peatlands: an ignored C sink and potential source. Glob. Change Biol. 15, 2311–2320 (2009).Article 

Google Scholar 
Garneau, M. et al. Holocene carbon dynamics of boreal and subarctic peatlands from Québec, Canada. Holocene 24, 1043–1053 (2014).Article 

Google Scholar 
Gorham, E. Northern peatlands: role in the carbon cycle and probable responses to climatic warming. Ecol. Appl. 1, 182–195 (1991).Article 

Google Scholar 
Turunen, J., Roulet, N. T., Moore, T. R. & Richard, P. J. H. Nitrogen deposition and increased carbon accumulation in ombrotrophic peatlands in eastern Canada. Glob. Biogeochem. Cycles 18, GB3002 (2004).Article 

Google Scholar 
Yu, Z. C. Northern peatland carbon stocks and dynamics: a review. Biogeosciences 9, 4071–4085 (2012).Article 

Google Scholar 
Poulter, B. et al. in Wetland Carbon And Environmental Management (eds Krauss, K. W., Zhu, Z. & Stagg, C. L.) 1–20 (American Geophysical Union, 2021).Honorio Coronado, E. et al. Intensive field sampling increases the known extent of carbon-rich Amazonian peatland pole forests. Environ. Res. Lett. 16, 074048 (2021).Article 

Google Scholar 
Sjögersten, S. et al. Tropical wetlands: a missing link in the global carbon cycle? Carbon cycling in tropical wetlands. Glob. Biogeochem. Cycles 28, 1371–1386 (2014).Article 

Google Scholar 
Griffis, T. J. et al. Hydrometeorological sensitivities of net ecosystem carbon dioxide and methane exchange of an Amazonian palm swamp peatland. Agric. For. Meteorol. 295, 108167 (2020).Article 

Google Scholar 
Kiew, F. et al. CO2 balance of a secondary tropical peat swamp forest in Sarawak, Malaysia. Agric. For. Meteorol. 248, 494–501 (2018).Article 

Google Scholar 
Hirano, T. et al. Effects of disturbances on the carbon balance of tropical peat swamp forests. Glob. Change Biol. 18, 3410–3422 (2012).Article 

Google Scholar 
Tang, A. C. I. et al. A Bornean peat swamp forest is a net source of carbon dioxide to the atmosphere. Glob. Change Biol. 26, 6931–6944 (2020).Article 

Google Scholar 
Deshmukh, C. S. et al. Conservation slows down emission increase from a tropical peatland in Indonesia. Nat. Geosci. 14, 484–490 (2021). This study presented measurements of CO2 and CH4 fluxes obtained using the eddy covariance method from both intact and degraded peat swamp forest in Sumatra, Indonesia, during the 2019 ENSO drought.Article 

Google Scholar 
Kiew, F. et al. Carbon dioxide balance of an oil palm plantation established on tropical peat. Agric. For. Meteorol. 295, 108189 (2020).Article 

Google Scholar 
McCalmont, J. et al. Short- and long-term carbon emissions from oil palm plantations converted from logged tropical peat swamp forest. Glob. Change Biol. 27, 2361–2376 (2021).Article 

Google Scholar 
Germer, J. & Sauerborn, J. Estimation of the impact of oil palm plantation establishment on greenhouse gas balance. Environ. Dev. Sustain. 10, 697–716 (2008).Article 

Google Scholar 
Lewis, K. et al. An assessment of oil palm plantation aboveground biomass stocks on tropical peat using destructive and non-destructive methods. Sci. Rep. 10, 2230 (2020).Article 

Google Scholar 
Wijedasa, L. S. Peat Swamp Forest Conservation in Southeast Asia. Thesis, National Univ. Singapore (2019).Moore, S. et al. Deep instability of deforested tropical peatlands revealed by fluvial organic carbon fluxes. Nature 493, 660–663 (2013).Article 

Google Scholar 
Cook, S. et al. Fluvial organic carbon fluxes from oil palm plantations on tropical peatland. Biogeosciences 15, 7435–7450 (2018).Article 

Google Scholar 
Waldron, S. et al. C mobilisation in disturbed tropical peat swamps: old DOC can fuel the fluvial efflux of old carbon dioxide, but site recovery can occur. Sci. Rep. 9, 11429 (2019).Article 

Google Scholar 
Brady, M. A. Organic Matter Dynamics of Coastal Peat Deposits in Sumatra, Indonesia. Thesis, Univ. British Columbia (1997).Jauhiainen, J., Limin, S., Silvennoinen, H. & Vasander, H. Carbon dioxide and methane fluxes in drained tropical peat before and after hhydrological restoration. Ecology 89, 3503–3514 (2008).Article 

Google Scholar 
Jauhiainen, J., Takahashi, H., Heikkinen, J. E. P., Martikainen, P. J. & Vasander, H. Carbon fluxes from a tropical peat swamp forest floor. Glob. Change Biol. 11, 1788–1797 (2005).Article 

Google Scholar 
Yule, C. M. & Gomez, L. N. Leaf litter decomposition in a tropical peat swamp forest in peninsular Malaysia. Wetl. Ecol. Manag. 17, 231–241 (2009).Article 

Google Scholar 
Swails, E., Hertanti, D., Hergoualc’h, K., Verchot, L. & Lawrence, D. The response of soil respiration to climatic drivers in undrained forest and drained oil palm plantations in an Indonesian peatland. Biogeochemistry 142, 37–51 (2019).Article 

Google Scholar 
Ishikura, K. et al. Carbon dioxide and methane emissions from peat soil in an undrained tropical peat swamp forest. Ecosystems 22, 1852–1868 (2019).Article 

Google Scholar 
Melling, L., Tan, C. Y., Goh, K. J. & Hatano, R. Soil microbial and root respirations from three ecosystems in tropical peatland of Sarawak, Malaysia. J. Oil Palm. Res. 25, 44–57 (2013).
Google Scholar 
Cooper, H. V. et al. Greenhouse gas emissions resulting from conversion of peat swamp forest to oil palm plantation. Nat. Commun. 11, 407 (2020).Article 

Google Scholar 
Girkin, N. T., Turner, B. L., Ostle, N. & Sjögersten, S. Root-derived CO2 flux from a tropical peatland. Wetl. Ecol. Manag. 26, 985–991 (2018).Article 

Google Scholar 
Dhandapani, S., Ritz, K., Evers, S., Yule, C. M. & Sjögersten, S. Are secondary forests second-rate? Comparing peatland greenhouse gas emissions, chemical and microbial community properties between primary and secondary forests in peninsular Malaysia. Sci. Total Environ. 655, 220–231 (2019).Article 

Google Scholar 
Dhandapani, S. et al. Land-use changes associated with oil palm plantations impact PLFA microbial phenotypic community structure throughout the depth of tropical peats. Wetlands 40, 2351–2366 (2020).Article 

Google Scholar 
Mishra, S. et al. Microbial and metabolic profiling reveal strong influence of water table and land-use patterns on classification of degraded tropical peatlands. Biogeosciences 11, 1727–1741 (2014).Article 

Google Scholar 
Mishra, S. et al. Degradation of Southeast Asian tropical peatlands and integrated strategies for their better management and restoration. J. Appl. Ecol. 58, 1370–1387 (2021). This paper reviews current understanding of intact and degraded peatlands in Southeast Asia and proposes an approach for peatland management and restoration involving explicit consideration of interacting ecological factors and the involvement of local communities.Article 

Google Scholar 
Carlson, K. M., Goodman, L. K. & May-Tobin, C. C. Modeling relationships between water table depth and peat soil carbon loss in Southeast Asian plantations. Environ. Res. Lett. 10, 074006 (2015).Article 

Google Scholar 
Carlson, K. M. et al. Committed carbon emissions, deforestation, and community land conversion from oil palm plantation expansion in West Kalimantan, Indonesia. Proc. Natl Acad. Sci. USA 109, 7559–7564 (2012).Article 

Google Scholar 
Couwenberg, J., Dommain, R. & Joosten, H. Greenhouse gas fluxes from tropical peatlands in south-east Asia. Glob. Change Biol. 16, 1715–1732 (2010).Article 

Google Scholar 
Evans, C. D. et al. Overriding water table control on managed peatland greenhouse gas emissions. Nature 593, 548–552 (2021). Using data for CO2 and CH4 fluxes from all major peatland biomes, this paper demonstrates that greenhouse gas emissions from drained agricultural peatlands could be greatly reduced by raising water levels closer to the peat surface while maintaining productive agricultural use.
Google Scholar 
Hooijer, A. et al. Current and future CO2 emissions from drained peatlands in Southeast Asia. Biogeosciences 7, 1505–1514 (2010).Article 

Google Scholar 
Hiraishi, T. et al. (eds) 2013 Supplement to the 2006 IPCC guidelines for national greenhouse gas inventories: wetlands (IPCC, 2014).Jauhiainen, J., Kerojoki, O., Silvennoinen, H., Limin, S. & Vasander, H. Heterotrophic respiration in drained tropical peat is greatly affected by temperature — a passive ecosystem cooling experiment. Environ. Res. Lett. 9, 105013 (2014).Article 

Google Scholar 
Manning, F. C., Kho, L. K., Hill, T. C., Cornulier, T. & Teh, Y. A. Carbon emissions from oil palm plantations on peat soil. Front. For. Glob. Change https://doi.org/10.3389/ffgc.2019.00037 (2019).Article 

Google Scholar 
Deshmukh, C. S. et al. Impact of forest plantation on methane emissions from tropical peatland. Glob. Change Biol. 26, 2477–2495 (2020).Article 

Google Scholar 
Wong, G. X. et al. How do land use practices affect methane emissions from tropical peat ecosystems? Agric. For. Meteorol. 282–283, 107869 (2020).Article 

Google Scholar 
Pangala, S. R. et al. Large emissions from floodplain trees close the Amazon methane budget. Nature 552, 230–234 (2017).Article 

Google Scholar 
Pangala, S. R., Moore, S., Hornibrook, E. R. C. & Gauci, V. Trees are major conduits for methane egress from tropical forested wetlands. N. Phytol. 197, 524–531 (2013).Article 

Google Scholar 
Hergoualc’h, K. et al. Spatial and temporal variability of soil N2O and CH4 fluxes along a degradation gradient in a palm swamp peat forest in the Peruvian Amazon. Glob. Change Biol. 26, 7198–7216 (2020).Article 

Google Scholar 
Teh, Y. A., Murphy, W. A., Berrio, J.-C., Boom, A. & Page, S. E. Seasonal variability in methane and nitrous oxide fluxes from tropical peatlands in the western Amazon basin. Biogeosciences 14, 3669–3683 (2017).Article 

Google Scholar 
Hoyos-Santillan, J. et al. Evaluation of vegetation communities, water table, and peat composition as drivers of greenhouse gas emissions in lowland tropical peatlands. Sci. Total Environ. 688, 1193–1204 (2019).Article 

Google Scholar 
van Haren, J. et al. A versatile gas flux chamber reveals high tree stem CH4 emissions in Amazonian peatland. Agric. For. Meteorol. 307, 108504 (2021).Article 

Google Scholar 
Sjögersten, S. et al. Temperature response of ex-situ greenhouse gas emissions from tropical peatlands: interactions between forest type and peat moisture conditions. Geoderma 324, 47–55 (2018).Article 

Google Scholar 
Girkin, N. T. et al. Spatial variability of organic matter properties determines methane fluxes in a tropical forested peatland. Biogeochemistry 142, 231–245 (2019).Article 

Google Scholar 
Girkin, N. T., Turner, B. L., Ostle, N. & Sjögersten, S. Composition and concentration of root exudate analogues regulate greenhouse gas fluxes from tropical peat. Soil. Biol. Biochem. 127, 280–285 (2018).Article 

Google Scholar 
Girkin, N. T., Vane, C. H., Turner, B. L., Ostle, N. J. & Sjögersten, S. Root oxygen mitigates methane fluxes in tropical peatlands. Environ. Res. Lett. 15, 064013 (2020).Article 

Google Scholar 
Jauhiainen, J., Silvennoinen, H., Könönen, M., Limin, S. & Vasander, H. Management driven changes in carbon mineralization dynamics of tropical peat. Biogeochemistry 129, 115–132 (2016).Article 

Google Scholar 
Wright, E. L. et al. Contribution of subsurface peat to CO2 and CH fluxes in a neotropical peatland. Glob. Change Biol. 17, 2867–2881 (2011).Article 

Google Scholar 
Prananto, J. A., Minasny, B., Comeau, L., Rudiyanto, R. & Grace, P. Drainage increases CO2 and N2O emissions from tropical peat soils. Glob. Change Biol. 26, 4583–4600 (2020).Article 

Google Scholar 
Peacock, M. et al. Global importance of methane emissions from drainage ditches and canals. Environ. Res. Lett. 16, 044010 (2021).Article 

Google Scholar 
Chuang, P.-C. et al. Methane fluxes from tropical coastal lagoons surrounded by mangroves, Yucatán, Mexico. J. Geophys. Res. Biogeosci. 122, 1156–1174 (2017).Article 

Google Scholar 
Jauhiainen, J. & Silvennoinen, H. Diffusion GHG fluxes at tropical peatland drainage canal water surfaces. Suoseura 63, 93–105 (2012).
Google Scholar 
Yupi, H. M., Inoue, T. & Bathgate, J. Concentrations, loads and yields of organic carbon from two tropical peat swamp forest streams in Riau Province, Sumatra, Indonesia. Mires Peat 18, 1–15 (2016).
Google Scholar 
Zhou, Y., Evans, C. D., Chen, Y., Chang, K. Y. W. & Martin, P. Extensive remineralization of peatland-derived dissolved organic carbon and ocean acidification in the Sunda Shelf Sea, Southeast Asia. J. Geophys. Res. Ocean. 126, e2021JC017292 (2021).
Google Scholar 
Alkhatib, M., Jennerjahn, T. C. & Samiaji, J. Biogeochemistry of the Dumai River estuary, Sumatra, Indonesia, a tropical black-water river. Limnol. Oceanogr. 52, 2410–2417 (2007).Article 

Google Scholar 
Gandois, L. et al. From canals to the coast: dissolved organic matter and trace metal composition in rivers draining degraded tropical peatlands in Indonesia. Biogeosciences 17, 1897–1909 (2020).Article 

Google Scholar 
Rixen, T. et al. The Siak, a tropical black water river in central Sumatra on the verge of anoxia. Biogeochemistry 90, 129–140 (2008).Article 

Google Scholar 
Miettinen, J., Hooijer, A., Vernimmen, R., Liew, S. C. & Page, S. E. From carbon sink to carbon source: extensive peat oxidation in insular Southeast Asia since 1990. Environ. Res. Lett. 12, 024014 (2017).Article 

Google Scholar 
Loisel, J. et al. Expert assessment of future vulnerability of the global peatland carbon sink. Nat. Clim. Chang. 11, 70–77 (2021).Article 

Google Scholar 
Boysen, L. R. et al. Global and regional effects of land-use change on climate in 21st century simulations with interactive carbon cycle. Earth Syst. Dyn. 5, 309–319 (2014).Article 

Google Scholar 
Sitch, S. et al. Recent trends and drivers of regional sources and sinks of carbon dioxide. Biogeosciences 12, 653–679 (2015).Article 

Google Scholar 
Mitchard, E. T. A. The tropical forest carbon cycle and climate change. Nature 559, 527–534 (2018).Article 

Google Scholar 
Naidu, D. G. T. & Bagchi, S. Greening of the Earth does not compensate for rising soil heterotrophic respiration under climate change. Glob. Change Biol. 27, 2029–2038 (2021).Article 

Google Scholar 
Li, W. et al. Future precipitation changes and their implications for tropical peatlands. Geophys. Res. Lett. 34, 01403 (2007).Article 

Google Scholar 
Barichivich, J. et al. Recent intensification of Amazon flooding extremes driven by strengthened Walker circulation. Sci. Adv. 4, eaat8785 (2018).Article 

Google Scholar 
Marengo, J. A. et al. Changes in climate and land use over the Amazon region: current and future variability and trends. Front. Earth Sci. 6, 228 (2018).Article 

Google Scholar 
Cobb, A. R. et al. How temporal patterns in rainfall determine the geomorphology and carbon fluxes of tropical peatlands. Proc. Natl. Acad. Sci. USA 114, E5187–E5196 (2017).Article 

Google Scholar 
Cai, W. et al. Increased variability of eastern Pacific El Niño under greenhouse warming. Nature 564, 201–206 (2018).Article 

Google Scholar 
Rifai, S. W., Li, S. & Malhi, Y. Coupling of El Niño events and long-term warming leads to pervasive climate extremes in the terrestrial tropics. Environ. Res. Lett. 14, 105002 (2019).Article 

Google Scholar 
Girkin, N. T. et al. Interactions between labile carbon, temperature and land use regulate carbon dioxide and methane production in tropical peat. Biogeochemistry 147, 87–97 (2020).Article 

Google Scholar 
Cole, L. E. S., Bhagwat, S. A. & Willis, K. J. Long-term disturbance dynamics and resilience of tropical peat swamp forests. J. Ecol. 103, 16–30 (2015).Article 

Google Scholar 
Weiss, D. et al. The geochemistry of major and selected trace elements in a forested peat bog, Kalimantan, SE Asia, and its implications for past atmospheric dust deposition. Geochim. Cosmochim. Acta 66, 2307–2323 (2002).Article 

Google Scholar 
Lähteenoja, O. & Page, S. High diversity of tropical peatland ecosystem types in the Pastaza-Marañón basin, Peruvian Amazonia. J. Geophys. Res. 116, G02025 (2011).
Google Scholar 
Roucoux, K. H. et al. Vegetation development in an Amazonian peatland. Palaeogeogr. Palaeoclimatol. Palaeoecol. 374, 242–255 (2013).Article 

Google Scholar 
Lampela, M., Jauhiainen, J. & Vasander, H. Surface peat structure and chemistry in a tropical peat swamp forest. Plant. Soil. 382, 329–347 (2014).Article 

Google Scholar 
Page, S. E., Rieley, J. O., Shotyk, Ø. W. & Weiss, D. Interdependence of peat and vegetation in a tropical peat swamp forest. Phil. Trans. R. Soc. Lond. B 354, 1885–1897 (1999).Article 

Google Scholar 
Sjögersten, S., Cheesman, A. W., Lopez, O. & Turner, B. L. Biogeochemical processes along a nutrient gradient in a tropical ombrotrophic peatland. Biogeochemistry 104, 147–163 (2011).Article 

Google Scholar 
Yule, C. M. Loss of biodiversity and ecosystem functioning in Indo-Malayan peat swamp forests. Biodivers. Conserv. 19, 393–409 (2010).Article 

Google Scholar 
Basilier, K. Moss-associated nitrogen fixation in some mire and coniferous forest environments around Uppsala, Sweden. Lindbergia 5, 84–88 (1979).
Google Scholar 
Ong, C. S. P., Juan, J. C. & Yule, C. M. Litterfall production and chemistry of Koompassia malaccensis and Shorea uliginosa in a tropical peat swamp forest: plant nutrient regulation and climate relationships. Trees 29, 527–537 (2015).Article 

Google Scholar 
Wüst, R. A. J. & Bustin, R. M. Opaline and Al–Si phytoliths from a tropical mire system of West Malaysia: abundance, habit, elemental composition, preservation and significance. Chem. Geol. 200, 267–292 (2003).Article 

Google Scholar 
Neuzil, S. G., Cecil, C. B., Kane, J. S. & Soedjono, K. in Modern and Ancient Coal-Forming Environments Vol. 286 (Geological Society of America, 1993).Too, C. C., Keller, A., Sickel, W., Lee, S. M. & Yule, C. M. Microbial community structure in a Malaysian tropical peat swamp forest: the influence of tree species and depth. Front. Microbiol. 9, 2859 (2018).Article 

Google Scholar 
Sulistiyanto, Y. Nutrient Dynamics in Different Sub-types of Peat Swamp Forest in Central Kalimantan, Indonesia. Thesis, Univ. Nottingham (2005).Hoyos Santillán, J. Controls of Carbon Turnover in Tropical Peatlands. Thesis, Univ. Nottingham (2014).Damman, A. W. H. Distribution and movement of elements in ombrotrophic peat bogs. Oikos 30, 480–495 (1978).Article 

Google Scholar 
Laiho, R. & Laine, J. Nitrogen and phosphorus stores in peatlands drained for forestry in Finland. Scand. J. For. Res. 9, 251–260 (1994).Article 

Google Scholar 
Wang, M., Moore, T. R., Talbot, J. & Riley, J. L. The stoichiometry of carbon and nutrients in peat formation. Glob. Biogeochem. Cycles 29, 113–121 (2015).Article 

Google Scholar 
Hodgkins, S. B. et al. Tropical peatland carbon storage linked to global latitudinal trends in peat recalcitrance. Nat. Commun. 9, 3640 (2018).Article 

Google Scholar 
Jackson, C. R., Liew, K. C. & Yule, C. M. Structural and functional changes with depth in microbial communities in a tropical Malaysian peat swamp forest. Microb. Ecol. 57, 402–412 (2009).Article 

Google Scholar 
Kolb, S. & Horn, M. A. Microbial CH4 and NO consumption in acidic wetlands. Front. Microbiol. 3, 78 (2012).Article 

Google Scholar 
Golovchenko, A. V., Tikhonova, E. Y. & Zvyagintsev, D. G. Abundance, biomass, structure, and activity of the microbial complexes of minerotrophic and ombrotrophic peatlands. Microbiology 76, 630–637 (2007).Article 

Google Scholar 
Martikainen, P. J., Nykänen, H., Crill, P. & Silvola, J. Effect of a lowered water table on nitrous oxide fluxes from northern peatlands. Nature 366, 51–53 (1993).Article 

Google Scholar 
Davidson, E. A., Keller, M., Erickson, H. E., Verchot, L. V. & Veldkamp, E. Testing a conceptual model of soil emissions of nitrous and nitric oxides. Bioscience 50, 667 (2000).Article 

Google Scholar 
Rubol, S., Silver, W. L. & Bellin, A. Hydrologic control on redox and nitrogen dynamics in a peatland soil. Sci. Total Environ. 432, 37–46 (2012).Article 

Google Scholar 
Jauhiainen, J. et al. Nitrous oxide fluxes from tropical peat with different disturbance history and management. Biogeosciences 9, 1337–1350 (2012).Article 

Google Scholar 
Könönen, M., Jauhiainen, J., Laiho, R., Kusin, K. & Vasander, H. Physical and chemical properties of tropical peat under stabilised land uses. Mires Peat 16, 1–13 (2015).
Google Scholar 
Chotimah, H., Jaya, A., Suparto, H., Saraswati, D. & Nawansyah, W. Utilizing organic fertilizers on two types of soil to improve growth and yield of Bawang Dayak (Eleutherine americana Merr). Agrivita J. Agric. Sci. 43, 164–173 (2021).
Google Scholar 
Mohidin, H. et al. Optimum levels of N, P, and K nutrition for oil palm seedlings grown in tropical peat soil. J. Plant. Nutr. 42, 1461–1471 (2019).Article 

Google Scholar 
Mutert, E., Fairhurst, T. H. & Von Uexküll, H. R. Agronomic management of oil palms on deep peat. Better. Crop. Int. 13, 22–27 (1999).
Google Scholar 
Hashim, S. A., Teh, C. B. S. & Ahmed, O. H. Influence of water table depths, nutrients leaching losses, subsidence of tropical peat soil and oil palm (Elaeis guineensis Jacq.) seedling growth. Malays. J. Soil. Sci. 23, 13–30 (2019).
Google Scholar 
Oktarita, S., Hergoualc’h, K., Anwar, S. & Verchot, L. V. Substantial N2O emissions from peat decomposition and N fertilization in an oil palm plantation exacerbated by hotspots. Environ. Res. Lett. 12, 104007 (2017).Article 

Google Scholar 
Hoyos-Santillan, J. et al. Root oxygen loss from Raphia taedigera palms mediates greenhouse gas emissions in lowland neotropical peatlands. Plant. Soil. 404, 47–60 (2016).Article 

Google Scholar 
Hatano, R. Impact of land use change on greenhouse gases emissions in peatland: a review. Int. Agrophys. 33, 167–173 (2019). This study reviews the impacts of changes in water-table level and nitrogen inputs on greenhouse gas emissions in tropical and northern peatlands and evaluates the optimal water-table level for minimizing emissions.Article 

Google Scholar 
Zawawi, N. Z. et al. The effect of nitrogen fertiliser on nitrous oxide emission in oil palm plantation. Proc. 15th Int. Peat Congress 355, 515–518 (2016).
Google Scholar 
Turetsky, M. R. et al. Global vulnerability of peatlands to fire and carbon loss. Nat. Geosci. 8, 11–14 (2015). This paper reviews peatland vulnerability to burning, fire-driven carbon emissions and current and future risks of peatland fires.Article 

Google Scholar 
Hu, Y. et al. Review of emissions from smouldering peat fires and their contribution to regional haze episodes. Int. J. Wildland Fire 27, 293–312 (2018).Article 

Google Scholar 
Huijnen, V. et al. Fire carbon emissions over maritime southeast Asia in 2015 largest since 1997. Sci. Rep. 6, 26886 (2016).Article 

Google Scholar 
Smith, T. E. L., Evers, S., Yule, C. M. & Gan, J. Y. In situ tropical peatland fire emission factors and their variability, as determined by field measurements in peninsula Malaysia. Glob. Biogeochem. Cycles 32, 18–31 (2018).Article 

Google Scholar 
Stockwell, C. E. et al. Field measurements of trace gases and aerosols emitted by peat fires in Central Kalimantan, Indonesia, during the 2015 El Niño. Atmos. Chem. Phys. 16, 11711–11732 (2016).Article 

Google Scholar 
Betha, R. et al. Chemical speciation of trace metals emitted from Indonesian peat fires for health risk assessment. Atmos. Res. 122, 571–578 (2013).Article 

Google Scholar 
Breulmann, G. et al. Heavy metals in emergent trees and pioneers from tropical forest with special reference to forest fires and local pollution sources in Sarawak, Malaysia. Sci. Total Environ. 285, 107–115 (2002).Article 

Google Scholar 
Othman, M. & Latif, M. T. Dust and gas emissions from small-scale peat combustion. Aerosol Air Qual. Res. 13, 1045–1059 (2013).Article 

Google Scholar 
See, S. W., Balasubramanian, R. & Wang, W. A study of the physical, chemical, and optical properties of ambient aerosol particles in Southeast Asia during hazy and nonhazy days. J. Geophys. Res. 111, D10S08 (2006).
Google Scholar 
Nikonovas, T., Spessa, A., Doerr, S. H., Clay, G. D. & Mezbahuddin, S. Near-complete loss of fire-resistant primary tropical forest cover in Sumatra and Kalimantan. Commun. Earth Env. 1, 65 (2020).Article 

Google Scholar 
Field, R. D., van der Werf, G. R. & Shen, S. S. P. Human amplification of drought-induced biomass burning in Indonesia since 1960. Nat. Geosci. 2, 185–188 (2009).Article 

Google Scholar 
Astiani, D., Taherzadeh, M. J., Gusmayanti, E., Widiastuti, T. & Burhanuddin, B. Local knowledge on landscape sustainable-hydrological management reduces soil CO2 emission, fire risk and biomass loss in west Kalimantan peatland, Indonesia. Biodiversiitas J. Biol. Divers. 20, 725–731 (2019).Article 

Google Scholar 
Cattau, M. E. et al. Sources of anthropogenic fire ignitions on the peat-swamp landscape in Kalimantan, Indonesia. Glob. Environ. Change 39, 205–219 (2016).Article 

Google Scholar 
Edwards, R. B., Naylor, R. L., Higgins, M. M. & Falcon, W. P. Causes of Indonesia’s forest fires. World Dev. 127, 104717 (2020).Article 

Google Scholar 
Field, R. D. & Shen, S. S. P. Predictability of carbon emissions from biomass burning in Indonesia from 1997 to 2006. J. Geophys. Res. Biogeosci. 113, G04024 (2008).Article 

Google Scholar 
Sloan, S., Locatelli, B., Wooster, M. J. & Gaveau, D. L. A. Fire activity in Borneo driven by industrial land conversion and drought during El Niño periods, 1982–2010. Glob. Environ. Change 47, 95–109 (2017).Article 

Google Scholar 
Page, S. E. et al. The amount of carbon released from peat and forest fires in Indonesia during 1997. Nature 420, 61–65 (2002).Article 

Google Scholar 
World Bank. The cost of fire: an economic analysis of Indonesia’s 2015 fire crisis (World Bank, 2016).Tacconi, L. Preventing fires and haze in Southeast Asia. Nat. Clim. Chang. 6, 640–643 (2016).Article 

Google Scholar 
Lupascu, M., Akhtar, H., Smith, T. E. L. & Sukri, R. S. Post-fire carbon dynamics in the tropical peat swamp forests of Brunei reveal long-term elevated CH4 flux. Glob. Change Biol. 26, 5125–5145 (2020).Article 

Google Scholar 
Milner, L. E. Influence of Fire on Peat Organic Matter from Indonesian Tropical Peatlands. Thesis, Univ. Leicester (2013).Saharjo, B. H. & Nurhayati, A. D. Changes in chemical and physical properties of hemic peat under fire-based shifting cultivation. Tropics 14, 263–269 (2005).Article 

Google Scholar 
Dhandapani, S. & Evers, S. Oil palm ‘slash-and-burn’ practice increases post-fire greenhouse gas emissions and nutrient concentrations in burnt regions of an agricultural tropical peatland. Sci. Total Environ. 742, 140648 (2020).Article 

Google Scholar 
Konecny, K. et al. Variable carbon losses from recurrent fires in drained tropical peatlands. Glob. Change Biol. 22, 1469–1480 (2016).Article 

Google Scholar 
Akhtar, H. et al. Significant sedge-mediated methane emissions from degraded tropical peatlands. Environ. Res. Lett. 16, 014002 (2020).
Google Scholar 
Rein, G. in Fire Phenomena and the Earth System (ed. Belcher, C. M.) 15–33 (Wiley, 2013).Graham, L. L. B. & Page, S. E. A limited seed bank in both natural and degraded tropical peat swamp forest: the implications for restoration. Mires Peat 22, 02 (2018).
Google Scholar 
Graham, E. B. et al. Microbes as engines of ecosystem function: when does community structure enhance predictions of ecosystem processes? Front. Microbiol. 7, 214 (2016).
Google Scholar 
Page, S. et al. Restoration ecology of lowland tropical peatlands in Southeast Asia: current knowledge and future research directions. Ecosystems 12, 888–905 (2009).Article 

Google Scholar 
Sazawa, K. et al. Impact of peat fire on the soil and export of dissolved organic carbon in tropical peat soil, Central Kalimantan, Indonesia. ACS Earth Space Chem. 2, 692–701 (2018).Article 

Google Scholar 
Dove, N. C. & Hart, S. C. Fire reduces fungal species richness and in situ mycorrhizal colonization: a meta-analysis. Fire Ecol. 13, 37–65 (2017).Article 

Google Scholar 
Veldkamp, E., Schmidt, M., Powers, J. S. & Corre, M. D. Deforestation and reforestation impacts on soils in the tropics. Nat. Rev. Earth Env. 1, 590–605 (2020).Article 

Google Scholar 
Qie, L. et al. Long-term carbon sink in Borneo’s forests halted by drought and vulnerable to edge effects. Nat. Commun. 8, 1966 (2017).Article 

Google Scholar 
Giesen, W. & Sari, E. N. N. Tropical peatland restoration report: the Indonesian case. MCA Indonesia https://doi.org/10.13140/RG.2.2.30049.40808 (2018).Article 

Google Scholar 
Dohong, A., Abdul Aziz, A. & Dargusch, P. A review of techniques for effective tropical peatland restoration. Wetlands 38, 275–292 (2018).Article 

Google Scholar 
Shell. Redd+ Katingan Mentaya, Indonesia. Shell https://www.shell.co.uk/motorist/make-the-change-drive-carbon-neutral/redd-plus-katingan-mentaya-indonesia.html (2021).Uda, S. K., Hein, L. & Sumarga, E. Towards sustainable management of Indonesian tropical peatlands. Wetl. Ecol. Manag. 25, 683–701 (2017).Article 

Google Scholar 
Wichtmann, W., Tanneberger, F., Wichmann, S. & Joosten, H. Paludiculture is paludifuture: climate, biodiversity and economic benefits from agriculture and forestry on rewetted peatland. Peatl. Int. 1, 48–51 (2010).
Google Scholar 
Giesen, W. in Tropical Peatland Eco-Management (eds Osaki, M., Tsuji, N., Foead, N. & Rieley, J.) 411–441 (Springer, 2021).Shurpali, N. J. et al. Atmospheric impact of bioenergy based on perennial crop (reed canary grass, Phalaris arundinaceae, L.) cultivation on a drained boreal organic soil. GCB Bioenergy 2, 130–138 (2010).
Google Scholar 
Lawson, I. T. et al. Improving estimates of tropical peatland area, carbon storage, and greenhouse gas fluxes. Wetl. Ecol. Manag. 23, 327–346 (2015).Article 

Google Scholar 
Anda, M. et al. Revisiting tropical peatlands in Indonesia: semi-detailed mapping, extent and depth distribution assessment. Geoderma 402, 115235 (2021).Article 

Google Scholar 
Saxon, E. C., Neuzil, S. G., Biladi, D. B. C., Kinser, J. & Sheppard, S. M. 3D mapping of lowland coastal peat domes in Indonesia. Mires Peat 27, 1–18 (2021).
Google Scholar 
Silvestri, S. et al. Quantification of peat thickness and stored carbon at the landscape scale in tropical peatlands: a comparison of airborne geophysics and an empirical topographic method. J. Geophys. Res. Earth Surf. 124, 3107–3123 (2019).Article 

Google Scholar 
Vernimmen, R. et al. Mapping deep peat carbon stock from a LiDAR based DTM and field measurements, with application to eastern Sumatra. Carbon Balance Manag. 15, 4 (2020).Article 

Google Scholar 
Andersen, R., Chapman, S. J. & Artz, R. R. E. Microbial communities in natural and disturbed peatlands: a review. Soil. Biol. Biochem. 57, 979–994 (2013).Article 

Google Scholar 
Morrison, E. S. et al. Characterization of bacterial and fungal communities reveals novel consortia in tropical oligotrophic peatlands. Microb. Ecol. 82, 188–201 (2020).Article 

Google Scholar 
Finn, D. R. et al. Methanogens and methanotrophs show nutrient-dependent community assemblage patterns across tropical peatlands of the Pastaza–Marañón Basin, Peruvian Amazonia. Front. Microbiol. 11, 746 (2020).Article 

Google Scholar 
Troxler, T. G. et al. Patterns of soil bacteria and canopy community structure related to tropical peatland development. Wetlands 32, 769–782 (2012).Article 

Google Scholar 
Tripathi, B. M. et al. Distinctive tropical forest variants have unique soil microbial communities, but not always low microbial diversity. Front. Microbiol. 7, 376 (2016).Article 

Google Scholar 
Kwon, M. J., Haraguchi, A. & Kang, H. Long-term water regime differentiates changes in decomposition and microbial properties in tropical peat soils exposed to the short-term drought. Soil. Biol. Biochem. 60, 33–44 (2013).Article 

Google Scholar 
Hadi, A. et al. Effects of land-use change in tropical peat soil on the microbial population and emission of greenhouse gases. Microbes Env. 16, 79–86 (2001).Article 

Google Scholar 
Kusai, N. A., Ayob, Z., Maidin, M. S. T., Safari, S. & Ahmad Ali, S. R. Characterization of fungi from different ecosystems of tropical peat in Sarawak, Malaysia. Rendiconti Lincei Sci. Fis. E 29, 469–482 (2018).Article 

Google Scholar 
Shuhada, S. N., Salim, S., Nobilly, F., Zubaid, A. & Azhar, B. Logged peat swamp forest supports greater macrofungal biodiversity than large-scale oil palm plantations and smallholdings. Ecol. Evol. 7, 7187–7200 (2017).Article 

Google Scholar 
Liu, B. et al. The microbial diversity and structure in peatland forest in Indonesia. Soil. Use Manag. 36, 123–138 (2020).Article 

Google Scholar 
Moyersoen, B., Becker, P. & Alexander, I. J. Are ectomycorrhizas more abundant than arbuscular mycorrhizas in tropical heath forests? N. Phytol. 150, 591–599 (2001).Article 

Google Scholar 
Muliyani, R. B., Sastrahidayat, I. R., Abdai, A. L. & Djauhari, S. Exploring ectomycorrhiza in peat swamp forest of Nyaru Menteng Palangka Raya Central Borneo. J. Biodivers. Environ. Sci. 5, 133–145 (2014).
Google Scholar 
Turjaman, M. et al. Improvement of early growth of two tropical peat-swamp forest tree species Ploiarium alternifolium and Calophyllum hosei by two arbuscular mycorrhizal fungi under greenhouse conditions. New Forests 36, 1–12 (2008).Article 

Google Scholar 
Tawaraya, K. et al. Arbuscular mycorrhizal colonization of tree species grown in peat swamp forests of Central Kalimantan, Indonesia. For. Ecol. Manag. 182, 381–386 (2003).Article 

Google Scholar 
Fenner, N. & Freeman, C. Drought-induced carbon loss in peatlands. Nat. Geosci. 4, 895–900 (2011).Article 

Google Scholar 
Yuwati, T. W. & Putri, W. S. Diversity of arbuscular mycorrhiza spores under Shorea balangeran (Korth.) Burck. plantation as bioindicator for the revegetation success. J. Galam 1, 15–26 (2020).Article 

Google Scholar 
Graham, L. L. B., Turjaman, M. & Page, S. E. Shorea balangeran and Dyera polyphylla (syn. Dyera lowii) as tropical peat swamp forest restoration transplant species: effects of mycorrhizae and level of disturbance. Wetl. Ecol. Manag. 21, 307–321 (2013).Article 

Google Scholar  More

Hu, C.-H. in Introduction to Roadside Geology of Ten Field Geology Excursion Routes in Northern Taiwan (ed Taiwan Normal University Department of Earth Science) 63–100 (Taiwan Normal University, 1987).Hu, C.-H. Fossil molluscs of Tongxiao Formation (Pleistocene), Longgang area, Miaoli County. Atlas Fossil Mollusca Taiwan 2, 689–754 (1992).
Google Scholar 
Hu, C.-H. Fossil molluscs of Tongxiao Formation (Pleistocene) in Baishatun and Touwo, Tongxiao village, Miaoli County. Atlas Fossil Mollusca Taiwan 1, 175–314 (1991).
Google Scholar 
Hayasaka, I. & Morishita, A. Notes on some fossil echinoids of Taiwan, II. Acta Geol. Taiwan. 1, 93–110 (1947).
Google Scholar 
Lin, Y.-J., Fang, J.-N., Chang, C.-C., Cheng, C.-C. & Lin, J. P. Stereomic microstructure of Clypeasteroida in thin section based on new material from Pleistocene strata in Taiwan. Terr. Atmos. Ocean. Sci. J. https://doi.org/10.3319/TAO.2021.07.28.01 (2021).Article 

Google Scholar 
Morishita, A. in Contributions to Celebrate Prof. Ichiro Hayasaka’s 76th Birthday 109–116 (1967).Wang, C.-C., Lin, C.-F. & Li, L.-C. Measurements on Late Pleistocene sand dollar Scaphechinus mirabilis from northern Taiwan. Annu. Rep. Central Geol. Surv. 72, 49–56 (1984).
Google Scholar 
Nisiyama, S. The echinoid fauna from Japan and adjacent regions. Part 2. Palaeontol. Soc. Jpn. Spec. Pap. 13, 1–491 (1968).
Google Scholar 
Kashenko, S. D. Effects of extreme changes of sea water temperature and salinity on the development of the sand dollar Scaphechinus mirabilis. Russ. J. Mar. Biol. 35, 422–430. https://doi.org/10.1134/s1063074009050083 (2009).Article 

Google Scholar 
Davies, A. J. & John, C. M. The clumped (13C–18O) isotope composition of echinoid calcite: Further evidence for “vital effects” in the clumped isotope proxy. Geochim. Cosmochim. Acta 245, 172–189. https://doi.org/10.1016/j.gca.2018.07.038 (2019).ADS 
CAS 
Article 

Google Scholar 
Chen, W.-S., Yeh, J.-J. & Syu, S.-J. Late Cenozoic exhumation and erosion of the Taiwan orogenic belt: New insights from petrographic analysis of foreland basin sediments and thermochronological dating on the metamorphic orogenic wedge. Tectonophysics 750, 56–69. https://doi.org/10.1016/j.tecto.2018.09.003 (2019).ADS 
Article 

Google Scholar 
Peng, T.-R., Wang, C.-H. & Chen, C. T. A. Oxygen and carbon isotopic studies of fossil Mollusca in the Kuokang Shell Bed, Paishatung, Miaoli. Spec. Publ. Central Geol. Surv. 4, 307–322 (1990).
Google Scholar 
Lee, C.-L. Biostratigraphy and sedimentary environments of Toukoshan Formation in Baishatun area, Miaoli MS thesis, National Central University (2000).Locarnini, R. A. et al. World Ocean Atlas 2018, Volume 1: Temperature. 1–52 (NOAA, 2019).Liew, P.-M. Quaternary stratigraphy in western Taiwan: Palynological correlation. Proc. Geol. Soc. China 31, 169–180 (1988).
Google Scholar 
Siddall, M., Rohling, E. J., Thompson, W. G. & Waelbroeck, C. Marine isotope stage 3 sea level fluctuations: Data synthesis and new outlook. Rev. Geophys. https://doi.org/10.1029/2007rg000226 (2008).Article 

Google Scholar 
LeGrande, A. N. & Schmidt, G. A. Global gridded data set of the oxygen isotopic composition in seawater. Geophys. Res. Lett. https://doi.org/10.1029/2006gl026011 (2006).Article 

Google Scholar 
Waelbroeck, C. et al. Sea-level and deep water temperature changes derived from benthic formainifera isotopic records. Quatern. Sci. Rev. 21, 295–305 (2002).ADS 
Article 

Google Scholar 
Epstein, S., Buchsbaum, R., Lowenstam, H. A. & Urey, H. C. Revised carbonate-water isotopic temperature scale. Bull. Geol. Soc. Am. 64, 1315–1326 (1963).Article 

Google Scholar 
Weber, J. N. & Raup, D. M. Fractionation of the stable isotopes of carbon and oxygen in marine calcareous organisms—the Echinoidea. Part II. Environmental and genetic factors. Geochim. Cosmochim. Acta 30, 705–736 (1966).ADS 
CAS 
Article 

Google Scholar 
Eiler, J. M. Paleoclimate reconstruction using carbonate clumped isotope thermometry. Quatern. Sci. Rev. 30, 3575–3588. https://doi.org/10.1016/j.quascirev.2011.09.001 (2011).ADS 
Article 

Google Scholar 
Takeda, S. Mechanism maintaining dense beds of the sand dollar Scaphechinus mirabilis in northern Japan. J. Exp. Mar. Biol. Ecol. 363, 21–27. https://doi.org/10.1016/j.jembe.2008.06.010 (2008).Article 

Google Scholar 
Takatsu, T., Nakatani, T., Miyamoto, T., Kooka, K. & Takahashi, T. Spatial distribution and feeding habits of Pacific cod (Gadus macrocephalus) larvae in Mutsu Bay, Japan. Fish. Oceanogr. 11, 90–101 (2002).Article 

Google Scholar 
Zhao, M., Huang, C.-Y. & Wei, K.-Y. A 28,000 year U37 K’ sea-surface temperature record of ODP Site 1202B, the southern Okinawa Trough. TAO 16, 45–56 (2005).ADS 
Article 

Google Scholar 
Jan, S., Tseng, Y.-H. & Dietrich, D. E. Sources of water in the Taiwan Strait. J. Oceanogr. 66, 211–221 (2010).Article 

Google Scholar 
Liao, E., Oey, L. Y., Yan, X.-H., Li, L. & Jiang, Y. The deflection of the China Coastal Current over the Taiwan Bank in winter. J. Phys. Oceanogr. 48, 1433–1450. https://doi.org/10.1175/jpo-d-17-0037.1 (2018).ADS 
Article 

Google Scholar 
Hu, J., Kawamura, H., Li, C., Hong, H. & Jiang, Y. Review on current and seawater volume transport through the Taiwan Strait. J. Oceanogr. 66, 591–610 (2010).Article 

Google Scholar 
Pico, T., Mitrovica, J. X., Ferrier, K. L. & Braun, J. Global ice volume during MIS 3 inferred from a sea-level analysis of sedimentary core records in the Yellow River Delta. Quatern. Sci. Rev. 152, 72–79. https://doi.org/10.1016/j.quascirev.2016.09.012 (2016).ADS 
Article 

Google Scholar 
Klein, R. T., Lohmann, K. C. & Kennedy, G. L. Elemental and isotopic proxies of paleotemperature and paleosalinity: Climate reconstruction of the marginal northeast Pacific ca. 80 ka. Geology 25, 363–366 (1997).ADS 
CAS 
Article 

Google Scholar 
Jarvis, I., Trabucho-Alexandre, J., Gröcke, D. R., Uličný, D. & Laurin, J. Intercontinental correlation of organic carbon and carbonate stable isotope records: Evidence of climate and sea-level change during the Turonian (Cretaceous). Depos. Rec. 1, 53–90. https://doi.org/10.1002/dep2.6 (2016).Article 

Google Scholar 
Chen, P. S. M. A study of the stratigraphy and molluscan fossils of the Tunghsiao area, Miaoli, Taiwan, R.O.C.. Bull. Malacol. Republic of China 4, 63–78 (1977).
Google Scholar 
Chen, W.-S. & Hsu, W.-J. The Pleistocene paleoenvironmental significance of the unearthed megafauna strata in Taiwan. Bull. Central Geol. Surv. 23, 137–163 (2010).
Google Scholar 
Chang, C. H. et al. The first archaic Homo from Taiwan. Nat. Commun. 6, 6037. https://doi.org/10.1038/ncomms7037 (2015).ADS 
CAS 
Article 
PubMed 

Google Scholar 
Cai, B.-Q. Fossil human humerus of Late Pleistocene from the Taiwan Straits. Acta Antrhopologica Sinica 20, 178–185 (2001).
Google Scholar 
Tong, H. & Patou-Mathis, M. Mammoth and other proboscideans in China during the Late Pleistocene. Deinsea 9, 421–428 (2003).
Google Scholar 
Koch, P. L. & Barnosky, A. D. Late quaternary extinctions: State of the debate. Annu. Rev. Ecol. Evol. Syst. 37, 215–250. https://doi.org/10.1146/annurev.ecolsys.34.011802.132415 (2006).Article 

Google Scholar 
Brook, B. W. & Bowman, D. M. J. S. Explaining the Pleistocene megafaunal extinctions: Models, chronologies, and assumptions. PNAS 99, 14624–14627 (2002).ADS 
CAS 
Article 

Google Scholar 
Barnosky, A. D., Koch, P. L., Feranec, R. S., Wing, S. L. & Shabel, A. B. Assessing the causes of Late Pleistocene extinctions on the continents. Science 306, 70–75 (2004).ADS 
CAS 
Article 

Google Scholar 
Ugan, A. & Byers, D. A global perspective on the spatiotemporal pattern of the Late Pleistocene human and woolly mammoth radiocarbon record. Quatern. Int. 191, 69–81. https://doi.org/10.1016/j.quaint.2007.09.035 (2008).Article 

Google Scholar 
Adlan, Q., Davies, A. J. & John, C. M. Effects of oxygen plasma ashing treatment on carbonate clumped isotopes. Rapid Commun. Mass Spectrom. 34, e8802. https://doi.org/10.1002/rcm.8802 (2020).CAS 
Article 
PubMed 

Google Scholar 
John, C. M. & Bowen, D. Community software for challenging isotope analysis: First applications of “Easotope” to clumped isotopes. Rapid Commun. Mass Spectrom. 30, 2285–2300 (2016).ADS 
CAS 
Article 

Google Scholar 
Bernasconi, S. M. et al. Background effects on Faraday collectors in gas-source mass spectrometry and implications for clumped isotope measurements. Rapid Commun. Mass Spectrom. 27, 603–612. https://doi.org/10.1002/rcm.6490 (2013).ADS 
CAS 
Article 
PubMed 

Google Scholar 
Bernasconi, S. M. et al. InterCarb: A community effort to improve interlaboratory standardization of the carbonate clumped isotope thermometer using carbonate standards. Geochem. Geophys. Geosyst. 22, e2020GC009588. https://doi.org/10.1029/2020GC009588 (2021).ADS 
CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
Anderson, N. T. et al. Unified clumped isotope thermometer calibration (0.5–1,100°C) using carbonate-based standardization. Geophys. Res. Lett. 48, e2020GL092069 (2021).ADS 
CAS 
Article 

Google Scholar 
Lee, H. et al. Young colonization history of a widespread sand dollar (Echinodermata; Clypeasteroida) in western Taiwan. Quatern. Int. 528, 120–129 (2019).Article 

Google Scholar 
Reimer, P. J. et al. IntCal13 and Marine13 radiocarbon age calibration curves 0–50,000 years cal BP. Radiocarbon 55, 1869–1887 (2013).CAS 
Article 

Google Scholar  More

Dobson, A., Lafferty, K. D., Kuris, A. M., Hechinger, R. F. & Jetz, W. Homage to Linnaeus: How many parasites? How many hosts?. Proc. Natl. Acad. Sci. 105, 11482–11489 (2008).ADS 
CAS 
Article 

Google Scholar 
Kuris, A. M. et al. Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454, 515–518 (2008).ADS 
CAS 
Article 

Google Scholar 
Seabloom, E. W. et al. The community ecology of pathogens: Coinfection, coexistence and community composition. Ecol. Lett. 18, 401–415 (2015).Article 

Google Scholar 
French, R. K. & Holmes, E. C. An ecosystems perspective on virus evolution and emergence. Trends Microbiol. 28, 165–175 (2020).CAS 
Article 

Google Scholar 
Hudson, P. J., Dobson, A. P. & Lafferty, K. D. Is a healthy ecosystem one that is rich in parasites?. Trends Ecol. Evol. 21, 381–385 (2006).Article 

Google Scholar 
Raffel, T. R., Martin, L. B. & Rohr, J. R. Parasites as predators: Unifying natural enemy ecology. Trends Ecol. Evol. 23, 610–618 (2008).Article 

Google Scholar 
Johnson, P. T. J. et al. When parasites become prey: Ecological and epidemiological significance of eating parasites. Trends Ecol. Evol. 25, 362–371 (2010).Article 

Google Scholar 
Frainer, A., McKie, B. G., Amundsen, P. A., Knudsen, R. & Lafferty, K. D. parasitism and the biodiversity-functioning relationship. Trends Ecol. Evol. 33, 260–268 (2018).Article 

Google Scholar 
Jephcott, T. G., Sime-Ngando, T., Gleason, F. H. & Macarthur, D. J. Host-parasite interactions in food webs: Diversity, stability, and coevolution. Food Webs 6, 1–8 (2016).Article 

Google Scholar 
Rohr, J. R. et al. Towards common ground in the biodiversity–disease debate. Nat. Ecol. Evol. 4, 24–33 (2020).Article 

Google Scholar 
Johnson, P. T. J., De Roode, J. C. & Fenton, A. Why infectious disease research needs community ecology. Science 349, 1259504 (2015).Article 

Google Scholar 
Marcogliese, D. J. & Cone, D. K. Food webs: A plea for parasites. Trends Ecol. Evol. 12, 320–325 (1997).CAS 
Article 

Google Scholar 
Chen, H.-W. et al. Network position of hosts in food webs and their parasite diversity. Oikos 117, 1847–1855 (2008).Article 

Google Scholar 
Lafferty, K. D., Dobson, A. P. & Kuris, A. M. Parasites dominate food web links. Proc. Natl. Acad. Sci. USA 103, 11211–11216 (2006).ADS 
CAS 
Article 

Google Scholar 
Lafferty, K. D. et al. Parasites in food webs: The ultimate missing links. Ecol. Lett. 11, 533–546 (2008).Article 

Google Scholar 
Dunne, J. A. The network structure of food webs. In Ecological Networks: Linking Structure to Dynamics (eds Pascual, M. & Dunne, J. A.) 27–28 (Oxford University Press, 2005).
Google Scholar 
Dunne, J. A., Williams, R. J. & Martinez, N. D. Network structure and biodiversity loss in food webs: Robustness increases with connectance. Ecol. Lett. 5, 558–567 (2002).Article 

Google Scholar 
Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H. & Dobson, A. P. The Ecology of Wildlife Diseases. (Oxford University Press, Oxford, 2002).
Google Scholar 
Anderson, R. M. & May, R. M. Infectious Diseases of Humans: Dynamics and Control (Oxford University Press, 1992).
Google Scholar 
McCallum, H. & Dobson, A. Detecting disease and parasite threats to endangered species and ecosystems. Trends Ecol. Evol. 10, 190–194 (1995).CAS 
Article 

Google Scholar 
De Castro, F. & Bolker, B. M. Parasite establishment and host extinction in model communities. Oikos 111, 501–513 (2005).Article 

Google Scholar 
McQuaid, C. F. & Britton, N. F. Parasite species richness and its effect on persistence in food webs. J. Theor. Biol. 364, 377–382 (2015).ADS 
Article 

Google Scholar 
Holt, R. D., Dobson, A. P., Begon, M., Bowers, R. G. & Schauber, E. M. Parasite establishment in host communities. Ecol. Lett. 6, 837–842 (2003).
Article 

Google Scholar 
Hatcher, M. J. & Dunn, A. M. Parasites in Ecological Communities: From Interactions to Ecosystems (Cambridge University Press, 2011).Book 

Google Scholar 
Dobson, A. Population dynamics of pathogens with multiple host species. Am. Nat. 164, S64–S78 (2004).Article 

Google Scholar 
McCann, K., Hastings, A. & Huxel, G. R. Weak trophic interactions and the balance of nature. Nature 395, 794–798 (1998).ADS 
CAS 
Article 

Google Scholar 
Neutel, A. M., Heesterbeek, J. A. P. & de Ruiter, P. C. Stability in real food webs: Weak links in long loops. Science 296, 1120–1123 (2002).ADS 
CAS 
Article 

Google Scholar 
Chen, X. & Cohen, J. E. Transient dynamics and food–web complexity in the Lotka–Volterra cascade model. Proc. R. Soc. Lond. Ser. B Biol. Sci. 268, 869–877 (2001).CAS 
Article 

Google Scholar 
May, R. M. Stability in multispecies community models. Math. Biosci. 12, 59–79 (1971).MathSciNet 
Article 

Google Scholar 
May, R. M. Will a large complex system be stable?. Nature 238, 413–414 (1972).ADS 
CAS 
Article 

Google Scholar 
Hilker, F. M. & Schmitz, K. Disease-induced stabilization of predator-prey oscillations. J. Theor. Biol. 255, 299–306 (2008).ADS 
MathSciNet 
Article 

Google Scholar 
Hethcote, H. W., Wang, W., Han, L. & Ma, Z. A predator–prey model with infected prey. Theor. Popul. Biol. 66, 259–268 (2004).Article 

Google Scholar 
Kooi, B. W., van Voorn, G. A. K. & Das, K. P. Stabilization and complex dynamics in a predator-prey model with predator suffering from an infectious disease. Ecol. Complex. 8, 113–122 (2011).Article 

Google Scholar 
Winemiller, K. O. Spatial and temporal variation in tropical fish trophic networks. Ecol. Monogr. 60, 331–367 (1990).Article 

Google Scholar 
Paine, R. T. Food-web analysis through field measurement of per capita interaction strength. Nature 355, 73–75 (1992).ADS 
Article 

Google Scholar 
Wootton, J. T. Estimates and tests of per capita interaction strength: Diet, abundance, and impact of intertidally foraging birds. Ecol. Monogr. 67, 45–64 (1997).Article 

Google Scholar 
Cohen, J. E., Briand, F. & Newman, C. M. Community Food Webs: Data and Theory (Springer, 1990).Book 

Google Scholar 
Mougi, A. Diversity of biological rhythm and food web stability. Biol. Lett. 17, 20200673 (2021).Article 

Google Scholar  More

Sol, D., Bacher, S., Reader, S. M. & Lefebvre, L. Brain size predicts the success of mammal species introduced into novel environments. Am. Nat. 172(Suppl. 1), S63–S71 (2008).PubMed 
Article 

Google Scholar 
González-Lagos, C., Sol, D. & Reader, S. M. Large-brained mammals live longer. J. Evol. Biol. 23, 1064–1074 (2010).PubMed 
Article 

Google Scholar 
Gonda, A., Herczeg, G. & Merilä, J. Evolutionary ecology of intraspecific brain size variation: A review. Ecol. Evol. 3(8), 2751–2764 (2013).PubMed 
PubMed Central 
Article 

Google Scholar 
Benson-Amram, S., Dantzer, B., Stricker, G., Swanson, E. M. & Holekamp, K. E. Brain size predicts problem-solving ability in mammalian carnivores. PNAS 113(9), 2532–2537 (2016).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Näslund, J., Aarestrup, K., Thomassen, S. T. & Johnsson, J. I. Early enrichment effects on brain development in hatchery-reared Atlantic salmon (Salmo salar): No evidence for a critical period. Can. J. Fish. Aquat. Sci. 69(9), 1481–1490 (2012).Article 

Google Scholar 
Logan, C. J., Kruuk, L. E. B., Stanley, R., Thompson, A. M. & Clutton-Brock, T. H. Endocranial volume is heritable and is associated with longevity and fitness in a wild mammal. R. Soc. Open Sci. 3(12), 160622 (2016).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Yamaguchi, N., Kitchener, A. C., Gilissen, E. & MacDonald, D. W. Brain size of the lion (Panthera leo) and the tiger (P. tigris): Implications for intrageneric phylogeny, intraspecific differences and the effects of captivity. Biol. J. Linn. Soc. 98, 85–93 (2009).Article 

Google Scholar 
Turschwell, M. P. & White, C. R. The effects of laboratory housing and spatial enrichment on brain size and metabolic rate in the eastern mosquitofish Gambusia holbrooki. Biol. Open. 5(3), 205–210 (2016).PubMed 
PubMed Central 
Article 

Google Scholar 
Welniak-Kaminska, M. et al. Volumes of brain structures in captive wild-type and laboratory rats: 7T magnetic resonance in vivo automatic atlas-based study. PLoS ONE 14(4), e0215348 (2019).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Guay, P. J., Parrott, M. & Selwood, L. Captive breeding does not alter brain volume in a marsupial over a few generations. Zoo Biol. 31, 82–86 (2012).PubMed 
Article 

Google Scholar 
Isler, K. et al. Endocranial volumes of primate species: Scaling analyses using a comprehensive and reliable data set. J. Hum. Evol. 55(6), 967–978 (2008).PubMed 
Article 

Google Scholar 
Burns, J. G., Saravanan, A. & Rodd, F. H. Rearing environment affects the brain size of guppies: Lab-reared guppies have smaller brains than wild-caught guppies. Ethol. 115(2), 122–133 (2009).Article 

Google Scholar 
Kruska, D. On the evolutionary significance of encephalization in some eutherian mammals: Effects of adaptive radiation, domestication, and feralization. Brain Behav. Evol. 65(2), 73–108 (2005).PubMed 
Article 

Google Scholar 
Logan, C. J. & Clutton-Brock, T. H. Validating methods for estimating endocranial volume in individual red deer (Cervus elaphus). Behav. Processes. 92, 143–146 (2013).PubMed 
Article 

Google Scholar 
Colby, A. E., Kimock, C. M. & Higham, J. P. Endocranial volume is variable and heritable, but not related to fitness, in a free-ranging primate. Sci. Rep. 11, 1–11 (2021).Article 
CAS 

Google Scholar 
Stuermer, I. W. & Wetzel, W. Early experience and domestication affect auditory discrimination learning, open field behaviour and brain size in wild Mongolian gerbils and domesticated Laboratory gerbils (Meriones unguiculatus forma domestica). Behav. Brain Res. 173, 11–21 (2006).PubMed 
Article 

Google Scholar 
Agnvall, B., Bélteky, J. & Jensen, P. Brain size is reduced by selection for tameness in red junglefowl-correlated effects in vital organs. Sci. Rep. 7(3306), 1–7 (2017).CAS 

Google Scholar 
Röhrs, M. & Ebinger, P. Wild is not really wild: Brain weight of wild and domestic mammals. Berl. Munch. Tierarztliche Wochenschrift. 112(6–7), 234–238 (1999).
Google Scholar 
Smith, B. P., Lucas, T. A., Norris, R. M. & Henneberg, M. Brain size/body weight in the dingo (Canis dingo): Comparisons with domestic and wild canids. Aust. J. Zool. 65(5), 292–301 (2017).Article 

Google Scholar 
Roberts, T., McGreevy, P. & Valenzuela, M. Human induced rotation and reorganization of the brain of domestic dogs. PLoS ONE 5(7), e11946 (2010).ADS 
PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Pollen, A. A. et al. Environmental complexity and social organization sculpt the brain in Lake Tanganyikan cichlid fish. Brain Behav. Evol. 70, 21–39 (2007).PubMed 
Article 

Google Scholar 
Kihslinger, R. L., Lema, S. C. & Nevitt, G. A. Environmental rearing conditions produce forebrain differences in wild Chinook salmon Oncorhynchus tshawytscha. Comp. Biochem. Physiol. 145(2), 145–151 (2006).CAS 
Article 

Google Scholar 
Guay, P. J. & Iwaniuk, A. N. Captive breeding reduces brain volume in waterfowl (Anseriformes). Condor 110(2), 276–284 (2008).Article 

Google Scholar 
Diamond, M. C., Ingham, C. A., Johnson, R. E., Bennett, E. L. & Rosenzweig, M. R. Effects of environment on morphology of rat cerebral cortex and hippocampus. J. Neurobiol. 7, 75–85 (1976).CAS 
PubMed 
Article 

Google Scholar 
Courtney Jones, S. K., Munn, A. J. & Byrne, P. G. Effect of captivity on morphology: Negligible changes in external morphology mask significant changes in internal morphology. R. Soc. Open Sci. 5(5), 1–13 (2018).Article 

Google Scholar 
Kruska, D. & Röhrs, M. Comparative-quantitative investigations on brains of feral pigs from the Galapagos Islands and of European domestic pigs. Z. Anat. Entwicklungsgesch. 144(1), 61–73 (1974).CAS 
PubMed 
Article 

Google Scholar 
Kruska, D. Changes of brain size in Tylopoda during phylogeny and caused by domestication. Verh. Dtsch. Zool. Ges. 75, 173–183 (1982).
Google Scholar 
Groves, C. P. Skull-changes due to captivity in certain Equidae. Z. Säugetierkd. 31, 44–46 (1966).
Google Scholar 
Groves, C. P. The skulls of Asian rhinoceroses: Wild and captive. Zoo Biol. 1, 251–261 (1982).Article 

Google Scholar 
Hollister, N. Some effects of environment and habit on captive lions. Proc. US. Natl. Mus. 53, 177–193 (1917).Article 

Google Scholar 
Price, E. O. Behavioral development in animals undergoing domestication. Appl. Anim. Behav. Sci. 65(3), 245–271 (1999).Article 

Google Scholar 
Wolff, J. Das Gesetz der Transformation der Knochen (A. Hirchwild, 1892).
Google Scholar 
Herring, S. W. Formation of the vertebrate face: Epigenetic and functional influences. Am. Zool. 33, 472–483 (1993).Article 

Google Scholar 
Wroe, S. & Milne, N. Convergence and remarkably consistent constraint in the evolution of carnivore skull shape. Evol. 61(5), 1251–1260 (2007).Article 

Google Scholar 
Damasceno, E. M., Hingst-Zaher, E. & Astúa, D. Bite force and encephalization in the Canidae (Mammalia: Carnivora). J. Zool. 290(4), 246–254 (2013).Article 

Google Scholar 
Van Valkenburgh, B. Deja vu: the evolution of feeding morphologies in the Carnivora. Integr. Comp. Biol. 47, 147–163 (2007).PubMed 
Article 

Google Scholar 
Van Valkenburgh, B. Carnivore dental adaptations and diet: A study of trophic diversity within guilds in Carnivore behavior, ecology, and evolution (ed. Gittleman, J. L.) 410–436 (Springer Science & Business Media, 1989).Slater, G. J., Dumont, E. R. & Van Valkenburgh, B. Implications of predatory specialization for cranial form and function in canids. J. Zool. 278(3), 181–188 (2009).Article 

Google Scholar 
Michaud, M., Veron, G. & Fabre, A. C. Phenotypic integration in feliform carnivores: Covariation patterns and disparity in hypercarnivores versus generalists. Evol. 74(12), 2681–2702 (2020).Article 

Google Scholar 
O’Regan, H. J. & Kitchener, A. C. The effects of captivity on the morphology of captive, domesticated and feral mammals. Mamm. Rev. 35, 215–230 (2005).Article 

Google Scholar 
Kapoor, V., Antonelli, T., Parkinson, J. A. & Hartstone-Rose, A. Oral health correlates of captivity. Res. Vet. Sci. 107, 213–219 (2016).PubMed 
Article 

Google Scholar 
Mitchell, D. R., Wroe, S., Ravosa, M. J. & Menegaz, R. A. More challenging diets sustain feeding performance: Applications toward the captive rearing of wildlife. Integr. Org. Biol. 3, 1–13 (2021).
Google Scholar 
Curtis, A. A., Orke, M., Tetradis, S. & Van Valkenburgh, B. Diet-related differences in craniodental morphology between captive-reared and wild coyotes, Canis latrans (Carnivora: Canidae). Biol. J. Linn. Soc. 123(3), 677–693 (2018).Article 

Google Scholar 
Siciliano-Martina, L., Light, J. E. & Lawing, A. M. Cranial morphology of captive mammals: A meta-analysis. Front. Zool. 18(4), 1–13 (2021).
Google Scholar 
Corruccini, R. S. & Beecher, R. M. Occlusal variation related to soft diet in a nonhuman primate. Science 218, 74–75 (1982).ADS 
CAS 
PubMed 
Article 

Google Scholar 
Ramirez Rozzi, F. V., González-José, R. & Pucciarelli, H. M. Cranial growth in normal and low-protein-fed Saimiri An environmental heterochrony. J. Hum. Evol. 49(4), 515–535 (2005).PubMed 
Article 

Google Scholar 
Taylor, A. B. & van Schaik, C. P. Variation in brain size and ecology in Pongo. J. Hum. Evol. 52, 59–71 (2007).PubMed 
Article 

Google Scholar 
AZA Canid TAG. Large Canid (Canidae) Care Manual. (Association of Zoos and Aquariums, 2012).Mexican Wolf Species Survival Plan. Mexican Gray Wolf Husbandry Manual: Guidelines for Captive Management (2009 edition). (Mexican Wolf Species Survival Plan and U.S. Fish and Wildlife Service, 2009).Carrera, R. et al. Comparison of Mexican wolf and coyote diets in Arizona and New Mexico. The J. Wildl. Manag. 72(2), 376–381 (2008).Article 

Google Scholar 
Reed, J. E. et al. Diets of free-ranging Mexican gray wolves in Arizona and New Mexico. Wildl. Soc. Bull. 34(4), 1127–1133 (2006).Article 

Google Scholar 
Kazimierska, K., Biel, W. & Witkowicz, R. Mineral composition of cereal and cereal-free dry dog foods versus nutritional guidelines. Molecules 25(21), 1–24 (2020).Article 
CAS 

Google Scholar 
Pezzali, J. G. & Aldrich, C. G. Effect of ancient grains and grain-free carbohydrate sources on extrusion parameters and nutrient utilization by dogs. J. Anim. Sci. 98(2), 3758–3767 (2019).Article 

Google Scholar 
Hartstone-Rose, A., Selvey, H., Villari, J. R., Atwell, M. & Schmidt, T. The three-dimensional morphological effects of captivity. PLoS ONE 9(11), 1–15 (2014).Article 
CAS 

Google Scholar 
Siciliano-Martina, L., Light, J. E. & Lawing, A. M. Changes in canid cranial morphology induced by captivity and conservation implications. Biol. Conserv. 257, 109143 (2021).Article 

Google Scholar 
Hedrick, P. W. & Fredrickson, R. Genetic rescue guidelines with examples from Mexican wolves and Florida panthers. Conserv. Genet. 11(2), 615–626 (2010).Article 

Google Scholar 
Greely, S. E. Mexican Wolf, Canis lupus baileyi, International Studbook 2018. Palm Desert, California. (2018).Kalinowski, S. T., Hedrick, P. W. & Miller, P. S. No inbreeding depression observed in Mexican and red wolf captive breeding programs. Conserv. Biol. 13(6), 1371–1377 (1999).Article 

Google Scholar 
Sakai, S. T., Whitt, B., Arsznov, B. M. & Lundrigan, B. L. Endocranial development in the coyote (Canis latrans) and gray wolf (Canis lupus): A computed tomographic study. Brain Behav. Evol. 91(2), 1–18 (2018).Article 

Google Scholar 
Van Valkenburgh, B. Skeletal and dental predictors of body mass in carnivores in Body size in mammalian paleobiology: estimation and biological implications (eds. Damuth, J. & MacFadden, B. J.) (Cambridge University Press, 1990).Rohlf, F. J. TPSDig2: a program for landmark development and analysis (2001).Siciliano-Martina, L., Light, J. E., Riley, D. G. & Lawing, A. M. One of these wolves is not like the other: morphological effects and conservation implications of captivity in Mexican wolves. Anim. Conserv. 25, 77–90 (2021).Article 

Google Scholar 
Zelditch, M. L., Donald, L., Swiderski, H., Sheets, D. & Fink, W. L. Geometric morphometrics for biologists: a primer. (Elsevier Academic Press, 2004).Coster, A. pedigree: Pedigree functions. R package version 1.4 (2013).Traylor-Holzer, K. (ed.). PMx user’s manual. Version 1.0. Apple Valley, MN: IUCN SSC Conservation Breeding Specialist Group. (2011).Thomason, J. J. Cranial strength in relation to estimated biting forces in some Mammals. Can. J. Zool. 69, 2326–2333 (1991).Article 

Google Scholar 
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods. 9(7), 676–682 (2012).CAS 
PubMed 
Article 

Google Scholar 
R Core Team R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. (2020).Cofran, Z. Brain size growth in wild and captive chimpanzees (Pan troglodytes). Am. J. Primat. 80(7), 1–8 (2018).Article 

Google Scholar 
Witzenberger, K. A. & Hochkirch, A. Ex situ conservation genetics: A review of molecular studies on the genetic consequences of captive breeding programmes for endangered animal species. Biodivers. Conserv. 20(9), 1843–1861 (2011).Article 

Google Scholar 
Gómez-Sánchez, D. et al. On the path to extinction: Inbreeding and admixture in a declining grey wolf population. Mole. Ecol. 27(18), 3599–3612 (2018).Article 

Google Scholar 
Elbroch, M. Animal skulls: a guide to North American species. (Stackpole Books, 2006).Conde, D. A., Flesness, N., Colchero, F., Jones, O. R. & Scheuerlein, A. An emerging role of zoos to conserve biodiversity. Science 331, 1390–1391 (2011).ADS 
CAS 
PubMed 
Article 

Google Scholar 
Prado, E. L. & Dewey, K. G. Nutrition and brain development in early life. Nutr. Rev. 72(4), 267–284 (2014).PubMed 
Article 

Google Scholar 
Hecht, E. E. et al. Neuromorphological changes following selection for tameness and aggression in the Russian farm-fox experiment. J. Neurosci. 41(28), 6144–6156 (2021).CAS 
PubMed Central 
Article 

Google Scholar 
Bennett, E. L., Rosenzweig, M. R. & Diamond, M. C. Rat brain: Effects of environmental enrichment on wet and dry weights. Science 163(3869), 825–826 (1969).ADS 
CAS 
PubMed 
Article 

Google Scholar 
Cummins, R. A., Walsh, R. N., Budtz-Olsen, O. E., Konstantinos, T. & Horsfall, C. R. Environmentally-induced changes in the brains of elderly rats. Nature 243(5409), 516–518 (1973).ADS 
CAS 
PubMed 
Article 

Google Scholar 
Welch, B. L., Brown, D. G., Welch, A. S. & Lin, D. C. Isolation, restrictive confinement or crowding of rats for one year. I. Weight, nucleic acids and protein of brain regions. Brain Res. 75, 71–84 (1974).CAS 
PubMed 
Article 

Google Scholar  More