Ecology

1.
Colwell, R. K., Brehm, G., Cardelus, C. L., Gilman, A. C. & Longino, J. T. Global warming, elevational range shifts, and lowland biotic attrition in the wet tropics. Science 322, 258–261 (2008).
ADS  CAS  PubMed  Article  Google Scholar 
2.
Soh, M. C. K. et al. Impacts of habitat degradation on tropical montane biodiversity and ecosystem services: A systematic map for identifying future research priorities. Front. For. Glob. Change. 2, 83 (2019).
Article  Google Scholar 

3.
Dolezal, J. et al. Vegetation dynamics at the upper elevational limit of vascular plants in Himalaya. Sci. Rep. 6, 24881 (2016).
ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

4.
Grant, E., Brand, A. B., De Wekker, S., Lee, T. R. & Wofford, J. Evidence that climate sets the lower elevation range limit in a high-elevation endemic salamander. Ecol. Evol. 8(15), 7553–7562 (2018).
PubMed  PubMed Central  Article  Google Scholar 

5.
Duclos, T. R., DeLuca, W. V. & King, D. I. Direct and indirect effects of climate on bird abundance along elevation gradients in the Northern Appalachian Mountains. Divers. Distrib. 25, 1670–1683 (2019).
Article  Google Scholar 

6.
Brehm, G., Süssenbach, D. & Fiedler, K. Unique elevational diversity patterns of geometrid moths in an Andean montane rainforest. Ecography 26, 456–466 (2003).
Article  Google Scholar 

7.
Axmacher, J. C. & Fiedler, K. Habitat type modifies geometry of elevational diversity gradients in geometrid moths (Lepidoptera Geometridae) on Mt Kilimanjaro, Tanzania. Trop. Zool. 21, 243–251 (2009).
Google Scholar 

8.
Rahbek, C. The elevational gradient of species richness: A uniform pattern. Ecography 18, 200–205 (1995).
Article  Google Scholar 

9.
Axmacher, J. C., Liu, Y., Wang, C., Li, L. & Yu, Z. Spatial α-diversity patterns of diverse insect taxa in Northern China: Lessons for biodiversity conservation. Biol. Conserv. 144, 2362–2368 (2011).
Article  Google Scholar 

10.
Li, J., Liu, H., Wu, Y., Zeng, L. & Huang, X. Spatial patterns and determinants of the diversity of Hemipteran insects in the Qinghai-Tibetan plateau. Front. Ecol. Evol. 7, 165 (2019).
ADS  Article  Google Scholar 

11.
Bender, I. M. A., Kissling, W. D. & Böhning-Gaese, K. Projected impacts of climate change on functional diversity of frugivorous birds along a tropical elevational gradient. Sci. Rep. 9, 17708 (2019).
ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

12.
Silveira, F. et al. Tropical mountains as natural laboratories to study global changes: A long-term ecological research project in a megadiverse biodiversity hotspot. Perspect. Plant Ecol. Evol. Syst. 38, 64–73 (2019).
Article  Google Scholar 

13.
Lohman, D. J. et al. Biogeography of the indo-australian archipelago. Annu. Rev. Ecol. Evol. Syst. 42(1), 205–226 (2011).
Article  Google Scholar 

14.
Kidane, Y. O., Steinbauer, M. J. & Beierkuhnlein, C. Dead end for endemic plant species? A biodiversity hotspot under pressure. Glob. Ecol. Conserv. 19, e00670 (2019).
Article  Google Scholar 

15.
Economic Planning Unit (EPU). Eleventh Malaysia Plan 2016–2020. Putrajaya: Prime minister’s department. (Malaysia, 2016).

16.
Sodhi N. S., & Brook, B. W. Southeast Asian Biodiversity in Crisis. (Cambridge University Press, 2006).

17.
Sodhi, N. S. et al. The state and conservation of Southeast Asian biodiversity. Biodivers. Conserv. 19, 317–328 (2010).
Article  Google Scholar 

18.
Laurance, W. F. Lessons from research for sustainable development and conservation in Borneo. Forests. 7, 314 (2016).
Article  Google Scholar 

19.
Schonberg, L. A., Longino, J. T., Nadkarni, N. M. & Yanoviak, S. P. Arboreal ant species richness in primary forest, secondary forest, and pasture habitats of a tropical montane landscape. Biotropica 36, 402–409 (2004).
Article  Google Scholar 

20.
Peh, K.S.-H. et al. Up in the clouds: Is sustainable use of tropical montane cloud forests possible in Malaysia. Bioscience 61, 27–38 (2011).
Article  Google Scholar 

21.
Hughes, A. C. Understanding the drivers of Southeast Asian biodiversity loss. Ecosphere 8(1), e01624 (2017).
Article  Google Scholar 

22.
Lessard, J.-P., Sackett, T. E., Reynolds, W. N., Fowler, D. A. & Sanders, N. J. Determinants of the detrital arthropod community structure: The effects of temperature and resources along an environmental gradient. Oikos 320, 333–343 (2011).
Article  Google Scholar 

23.
Cronin, D. T., Libalah, M. B., Bergl, R. A. & Hearn, G. W. Biodiversity and conservation of tropical montane ecosystems in the Gulf of Guinea, West Africa. Arct. Antarct. Alp. Res. 46(4), 891–904 (2014).
Article  Google Scholar 

24.
Nowrouzi, S. et al. Ant diversity and distribution along elevation gradients in the Australian wet tropics: The importance of seasonal moisture stability. PLoS ONE 11(4), e0153420 (2016).
PubMed  PubMed Central  Article  CAS  Google Scholar 

25.
Perillo, L. N., Neves, F. D. S., Antonini, Y. & Martins, R. P. Compositional changes in bee and wasp communities along neotropical mountain altitudinal gradient. PLoS ONE 12(7), e0182054 (2017).
PubMed  PubMed Central  Article  CAS  Google Scholar 

26.
Maicher, V. et al. Seasonal shifts of biodiversity patterns and species elevation ranges of butterflies and moths along a complete rainforest elevational gradient on Mount Cameroon. J. Biogeogr. 47, 342–354 (2020).
Article  Google Scholar 

27.
Rahbek, C. et al. Building mountain biodiversity: Geological and evolutionary processes. Science 365, 1114–1119 (2019).
ADS  CAS  PubMed  Article  Google Scholar 

28.
Musthafa, M. M., Abdullah, F. & Sanchez, U. Comparative study of spatial patterns and ecological niches of beetles in two Malaysian mountains elevation gradients. J. Insect Conserv. 22(5–6), 757–769 (2018).
Article  Google Scholar 

29.
Musthafa, M. M. & Abdullah, F. Beetles species richness along environmental gradients at montane ecosystem in Fraser’s Hill, peninsular Malaysia. Sains Malays. 48(7), 1395–1407 (2019).
Article  Google Scholar 

30.
Musthafa, M. M. & Abdullah, F. Coleoptera of genting Highland, Malaysia: Species richness and diversity along the elevations. Arxius de Miscel·lània Zoològica. 17, 123–144 (2019).

31.
Nazaruddin, D. A., Hassan, H. & Sanusi, A. F. A. Some geological attractions of mount chamah area, Kelantan, Malaysia. J. Appl. Sci. Res. 9(3), 1298–1304 (2013).
Google Scholar 

32.
Kumaran, J. V. et al. Diversity and conservation status of small mammals in Kelantan, Malaysia. Songklanakarin J. Sci. Technol. 38(2), 213–220 (2016).
Google Scholar 

33.
Aweng, E. R., Suhaimi, O. & Izzati, S. N. Benthic macroinvertebrate community structure and distribution in Sungai Pichong, Gunung Chamah, Kelantan, Malaysia. Am. Int. J. Contemp. Res. 2(1), 163–167 (2012).
Google Scholar 

34.
Sulaiman, N., Bakri, M. A. M., Kahar, K. M., Yaacob, M. Z. & Boler, I. Moth fauna (Lepidoptera: Heterocera) of Gunung Tebu forest reserve, Terengganu, Malaysia. Malayan Nat. J. 66(4), 376–389 (2014).
Google Scholar 

35.
Nordin, R., Malek, I. A. & Manohar, M. Rain forest recreation zone planning using geo spatial tools. Pertanika J. Trop. Agric. Sci. 36, 181–194 (2013).
Google Scholar 

36.
Grytnes, J. A., & McCain, C. M. Elevational trends in biodiversity. (ed. Simon, A.L.) Encyclopedia of Biodiversity. 1–8 (USA, 2007).

37.
Lazarina, M. et al. Diversity patterns of different life forms of plants along an elevational gradient in Crete, Greece. Diversity. 11, 200 (2019).
Article  Google Scholar 

38.
Masse, P. S. M. & Makon, S. D. Effects of human disturbance and altitudinal gradient on Myriapod species richness and abundance at Mount Kala, central Cameroon. Afr. Zool. 54(4), 215–223 (2019).
Article  Google Scholar 

39.
Zhou, Y. et al. The species richness pattern of vascular plants along a tropical elevational gradient and the test of elevational rapoport’s rule depend on different life-forms and phytogeographic affinities. Ecol. Evol. 9, 4495–4503 (2019).
PubMed  PubMed Central  Article  Google Scholar 

40.
Deng, W., Wang, J. & Scott, M. B. Sampling methods affect nematode-trapping fungi biodiversity patterns across an elevational gradient. BMC Microbioogyl. 20, 15 (2020).
Article  Google Scholar 

41.
Skvarla, M. J. & Dowling, A. P. G. A comparison of trapping techniques (Coleoptera: Carabidae, Buprestidae, Cerambycidae, and Curculionoidea excluding Scolytinae). J. Insect Sci. 17(1), 7–20 (2017).
PubMed  PubMed Central  Article  CAS  Google Scholar 

42.
Basset, Y. et al. IBISCA-Panama, a large-scale study of arthropod beta-diversity and vertical stratification in a lowland rainforest: Rationale, study sites and field protocols. Bulletin de l’Institut Royal des Sciences Naturelles de Belgique. 77, 36–69 (2007).
Google Scholar 

43.
Nizar, N. B. M. Geology of the jelebu area, negeri sembilan with emphasis on geomorphological analysis. BSc Thesis University of Malaya, (Malaysia, 2016).

44.
Surjono, S. S., Leman, M. S., Ali, C. A., Mohamed, K. R., & Mada, M. F. H. Petrogenesis and depositional environment of paleozoic sedili and pengerang volcaniclastics in east Johor Basin, peninsular Malaysia. E3S Web of Conferences. 76, 04009 (2019).

45.
Aweng-Eh, R., Ismid-Said, M., Maketab-Mohamed, M. & Ahmad-Abas, K. Macrobenthic community structure and distribution in the Gunung Belumut recreational forest, Kluang, Johor, Malaysia. Aust. J. Basic Appl. Sci. 4(8), 3904–3908 (2010).
Google Scholar 

46.
Abdullah, F., & Sabri, M.S.M. Beetle fauna of Gunung Besar Hantu forest reserve, Jelebu. In Siri kepelbagaian biologi hutan: Hutan Gunung Besar Hantu, Negeri Sembilan: Pengurusan hutan, persekitaran fizikal dan kepelbagaian (eds. Rahman, A. et al.) Biology, 199–214 (Jabatan Perhutanan Semenanjung, 2014).

47.
Betz, O., Srisuka, W. & Puthz, V. Elevational gradients of species richness, community structure, and niche occupation of tropical rove beetles (Coleoptera: Staphylinidae: Steninae) across mountain slopes in Northern Thailand. Ecol. Evol. 34, 193–216 (2020).
Article  Google Scholar 

48.
Zhang, W., Huang, D., Wang, R., Liu, J. & Du, N. Altitudinal patterns of species diversity and phylogenetic diversity across temperate mountain forests of Northern China. PLoS ONE 11(7), e0159995 (2016).
PubMed  PubMed Central  Article  CAS  Google Scholar 

49.
Kontopanou, A. & Panitsa, M. Habitat islands on the Aegean islands (Greece): Elevational gradient of chasmophytic diversity, endemism, phytogeographical patterns and need for monitoring and conservation. Diversity. 12(1), 33 (2020).
Article  Google Scholar 

50.
Jordal, B. H., Normark, B. B., Farrell, B. D. & Kirkendalld, L. R. Extraordinary haplotype diversity in haplodiploid inbreeders: Phylogenetics and evolution of the bark beetle genus Coccotrypes. Mol. Phylogenet. Evol. 23, 171–188 (2002).
CAS  PubMed  Article  PubMed Central  Google Scholar 

51.
Lassau, S. A., Hochuli, D. F., Cassis, G. & Reid, C. A. M. Effects of habitat complexity on forest beetle diversity: Do functional groups respond consistently. Divers. Distrib. 11, 73–82 (2005).
Article  Google Scholar 

52.
Cosovic, M., Bugalho, M. N., Thom, D. & Borges, J. G. Stand structural characteristics are the most practical biodiversity indicators for forest management planning in Europe. Forests. 11, 343 (2020).
Article  Google Scholar 

53.
Jankowski, J. E., Ciecka, A. L., Meyer, N. Y. & Rabenold, K. N. Beta diversity along environmental gradients: Implications of habitat specialization in tropical montane landscapes. J. Anim. Ecol. 78, 315–327 (2009).
PubMed  Article  PubMed Central  Google Scholar 

54.
Novotny, V. & Weiblen, G. D. From communities to continents: Beta diversity of herbivorous insects. Ann. Zool. Fenn. 42, 463–475 (2005).
Google Scholar 

55.
Legendre, P. Interpreting the replacement and richness difference components of beta diversity. Glob. Ecol. Biogeogr. 23, 1324–1334 (2014).
Article  Google Scholar 

56.
Nguyen, D. T. & Gómez-Zurita, J. Subtle ecological gradient in the tropics triggers high species-turnover in a local geographical scale. PLoS ONE 11(6), e0156840 (2016).
PubMed  PubMed Central  Article  CAS  Google Scholar 

57.
Antão, L. H., McGill, B., Magurran, A. E., Soares, A. M. V. M. & Dornelas, M. β-diversity scaling patterns are consistent across metrics and taxa. Ecography 42, 1012–1023 (2019).
Article  Google Scholar 

58.
Bevilacqua, S. & Terlizzi, A. Nestedness and turnover unveil inverse spatial patterns of compositional and functional β-diversity at varying depth in marine benthos. Divers. Distrib. 26, 743–757 (2020).
Article  Google Scholar 

59.
da Silva, P. G., Hernández, M. I. M. & Heino, J. Disentangling the correlates of species and site contributions to beta diversity in dung beetle assemblages. Divers. Distrib. 24, 1674–1686 (2018).
Article  Google Scholar 

60.
Feeley, K. J. & Silman, M. R. Biotic attrition from tropical forests correcting for truncated temperature niches. Glob. Change Biol. 16, 1830–1836 (2010).
ADS  Article  Google Scholar 

61.
Brodie, J. F. et al. Lowland biotic attrition revisited: Body size and variation among climate change “winners” and “losers”. Proc. Biol. Sci. 284(1847), 20162335 (2017).
PubMed  PubMed Central  Google Scholar 

62.
Penaloza, R. J. M. et al. Consequences of habitat fragmentation on genetic structure of Chamaedorea alternans (Arecaceae) palm populations in the tropical rain forests of los Tuxtlas, Veracruz, Mexico. Revista Mexicana de Biodiversidad. 87(3), 990–1001 (2016).
Article  Google Scholar 

63.
Villacampa, J., Whitworth, A., Allen, L. & Malo, J. E. Altitudinal differences in alpha, beta and functional diversity of an amphibian community in a biodiversity hotspot. Neotrop. Biodivers. 5(1), 60–68 (2019).
Article  Google Scholar 

64.
Kiew, R. The Encyclopedia of Malaysia. Vol. II. Plants Montane Forests (Archipelago Press, 1998).

65.
Shahrudin, S. et al. An addition of reptiles of Gunung inas, Kedah, Malaysia. Russ. J. Herpetol. 20(3), 171–180 (2013).
Google Scholar 

66.
Chan, N. W. Degradation of the highland areas in Malaysia. Effects on water resources. Consumer Association of Penang. (ed. Tanah air ku: Land issues in Malaysia). 66–86 (Malaysia, 2000).

67.
Chua, L. S. L. & Saw, L. G. Plants of Krau. FRIM Res. Pam. 126, 227 (2006).
Google Scholar 

68.
Ramly, F. N., & Ramli, R. Diversity of understorey birds in Virgin and logged forests of Gunung Angsi forest reserve, Negeri (ed. Sembilan, H. et al.). Harnessing the Potential of Biodiversity, Simposium Biology. 65–68 (Malaysia, 2009).

69.
Sofiah, M. S. Komposisi, kepelbagaian dan biojisim pokok di Hutan Lipur Gunung Belumut, Kluang (Univeristi Kebangsaan, 2010).
Google Scholar 

70.
Ashton P. S., Okuda T., Manokaran N. Pasoh research, past and present. In Pasoh (eds. Okuda T. et al.), 1–13 (Springer, 2003).

71.
Rayan, D. M. & Mohamed, S. W. The importance of selectively logged forests for tiger Panthera tigris conservation: A population density estimates in Peninsular Malaysia. Oryx 43(1), 48–51 (2009).
Article  Google Scholar 

72.
Saito, M. A new species of the genus Tomoderus (Coleoptera, Anthicidae) from the Ryukyu Islands, Southwest Japan. Elytra. 31, 321–323 (2003).
Google Scholar 

73.
Mohamedsaid, M. S. (ed. Catalogue of the Malaysian Chrysomelidae Insecta: Coleoptera). (Bulgeria, 2004).

74.
Kirejtshuk, A. G. On the fauna of Nitidulidae (Insecta, Coleoptera) from Taiwan with some taxonomical notes. Annales Historico-Naturales Musei Nationalis Hungarici. 97, 51–113 (2005).
Google Scholar 

75.
Naomi, S Taxonomic revision of the genus Stenus latreille, 1797 (Coleoptera, Staphylinidae, steninae) of Japan: Species group of S. indubius Sharp. Jpn. J. Syst. Entomol. 12(1), 39–120 (2006).

76.
Schawaller, W. Revision of the oriental species of the genus Bradymerus perroud, with descriptions of 29 new species (Coleoptera: Tenebrionidae). Stuttgarter beiträge zur Naturkunde. 4, 1–64 (2006).
Google Scholar 

77.
Schawaller, W. Two new species and new records of the genus Spinolyprops Pic, 1917 from the oriental region (Coleoptera, Tenebrionidae, Lupropini). ZooKeys. 243, 83–94 (2012).
Article  Google Scholar 

78.
Schimmel, R. & Tarnawski, D. Monograph of the subtribe Elaterina (Insecta: Coleoptera: Elateridae: Elaterinae). Genus 21(3), 325–487 (2010).
Google Scholar 

79.
Assing, V. Four new species and additional records of Palaearctic Sunius, with two new synonymies (Coleoptera: Staphylinidae: Paederinae). Beiträge zur Entomologie. 58, 455–470 (2008).
Article  Google Scholar 

80.
Grimm, R. Guanobius borneensis n. gen., n. sp. from Borneo (Coleoptera: Tenebrionidae: Alphitobiini). Stuttgarter Beiträge zur Naturkunde A, Neue Serie. 1, 375–379 (2008).

81.
Batelka, J. Clinopalpus hanae, a new genus and species of ripiphorid beetle from Malaysia (Coleoptera: Ripiphoridae: Pelecotominae). Acta Entomologica Musei Nationalis Pragae 49(1), 239–245 (2009).
Google Scholar 

82.
Gerstmeier, R. Taxonomic supplement to a revision of Omadius Laporte 1836 (Mawdsley 2006) (Coleoptera: Cleridae). Annales de la Société Entomologique de France. 45(2), 135–144 (2009).
Article  Google Scholar 

83.
Sittichaya, W., Beaver, R. A., Liu, L.-Y. & Ngampongsai, A. An illustrated key to powder post beetles (Coleoptera, Bostrichidae) associated with rubberwood in Thailand, with new records and a checklist of species found in Southern Thailand. ZooKeys. 26, 33–51 (2009).
Article  Google Scholar 

84.
Hlaváč, P., Newton, A. F. & Maruyama, M. World catalogue of the species of the tribe Lomechusini (Staphylinidae: Aleocharinae). Zootaxa 3075, 1–151 (2011).
Google Scholar 

85.
Prathapan, K. D. & Viraktamath, C. A. A new species of Longitarsus latreille, 1829 (Coleoptera, Chrysomelidae, Galerucinae) pupating inside stem aerenchyma of the hydrophyte host from the Oriental Region. ZooKeys. 87, 1–10 (2011).
Article  Google Scholar 

86.
Ryvkin, A. B. Contributions to the knowledge of Stenus (Nestus) species of the crassus group (Insecta: Coleoptera: Staphylinidae: Steninae). Four new species from the Russian far east with taxonomic notes. Baltic J. Coleopterol. 11(1), 57–72 (2011).

87.
Caterino, M. S. & Tishechkin, A. K. A systematic revision of Baconia Lewis (Coleoptera, Histeridae, Exosternini). ZooKeys. 343, 1–297 (2013).
Article  Google Scholar 

88.
Pace, R. New distributional data, new species and three new genera of Aleocharinae from Malaysia, Vietnam and Taiwan (Coleoptera: Staphylinidae). Trop. Zool. 26(1), 33–63 (2013).
Article  Google Scholar 

89.
Shi, H., Zhou, H. & Liang, H. Taxonomic synopsis of the subtribe Physoderina (Coleoptera, Carabidae, Lebiini), with species revisions of eight genera. Zookeys. 284, 1–129 (2013).
Article  Google Scholar 

90.
Mertlik, J. & Németh, T. Distributional notes on Lacon nadaii and L. unicolor (Coleoptera: Elateridae). Elateridarium. 8, 61–66 (2013).
Google Scholar 

91.
Filippini, V., Micó, E. & Galante, E. Checklist and identification key of Anomalini (Coleoptera, Scarabaeidae, Rutelinae) of Costa Rica. ZooKeys. 621, 63–136 (2016).
Article  Google Scholar 

92.
Anzaldo, S. S. Review of the genera of Conoderinae (Coleoptera, Curculionidae) from North America, Central America, and the Caribbean. ZooKeys. 683, 51–138 (2017).
Article  Google Scholar 

93.
Makranczy, G. Review of the Anotylus Cimicoides species group (Coleoptera: Staphylinidae: Oxytelinae). Acta Zool. Acad. Sci. Hung. 63(2), 143–262 (2017).
Article  Google Scholar 

94.
Sasakawa, K., Kim, J.-K., Kim, J.-K. & Kubota, K. Morphological phylogeny and biogeography of the Pterostichus raptor species group (Coleoptera: Carabidae) of ground beetles, endemic to the Korean Peninsula and adjacent islands. J. Asia-Pac. Entomol. 20, 7–12 (2017).
Article  Google Scholar 

95.
Murakami, H. A new species of the genus Cladiscus chevrolat, 1843 (Coleoptera: Cleridae: Tillinae) from Borneo, Malaysia. Jpn. J. Syst. Entomol. 23(2), 235–238 (2017).
Google Scholar 

96.
Murakami, H. & Cheong, L. F. A new species of the genus Allochotes westwood, 1875 (Coleoptera: Cleridae: Orthopleurinae) from Malay Peninsula. Jpn. J. Syst. Entomol. 24(2), 221–224 (2018).
Google Scholar 

97.
Moore, M. R., Cave, R. D. & Branham, M. A. Synopsis of the cyclocephaline scarab beetles (Coleoptera, Scarabaeidae, Dynastinae). ZooKeys. 745, 1–99 (2018).
Article  Google Scholar 

98.
Chao, A. & Jost, L. Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology 93, 2533–2547 (2012).
PubMed  Article  PubMed Central  Google Scholar 

99.
Jost, L. Entropy and diversity. Oikos 113, 363–374 (2006).
Article  Google Scholar 

100.
Moreno, C. E. et al. Measuring biodiversity in the Anthropocene: A simple guide to helpful methods. Biodivers. Conserv. 26(12), 2993–2998 (2017).
Article  Google Scholar 

101.
R Development Core Team. A language and environment for statistical computing. R. Foundation for Statistical Computing. (Austria, 2015)

102.
Dufrêne, M. & Legendre, P. Species assemblages and indicator species: The need for a flexible asymmetrical approach. Ecol. Monogr. 67, 345–366 (1997).
Google Scholar 

103.
De Cáceres, M. & Legendre, P. Associations between species and groups of sites: Indices and statistical inference. Ecology 90, 3566–3574 (2009).
PubMed  Article  Google Scholar 

104.
De Cáceres, M., Legendre, P. & Moretti, M. Improving indicator species analysis by combining groups of sites. Oikos 119, 1674–1684 (2010).
Article  Google Scholar 

105.
De Cáceres, M., Legendre, P., Wiser, S. K. & Brotons, L. Using species combinations in indicator value analyses. Methods Ecol. Evol. 3, 973–982 (2012).
Article  Google Scholar 

106.
Anderson, M. J. & Walsh, D. C. I. What null hypothesis are you testing? PERMANOVA, ANOSIM and the mantel test in the face of heterogeneous dispersions. Ecol. Monogr. 83, 557–574 (2013).
Article  Google Scholar 

107.
Clarke, K. R., & Gorley, R. N. PRIMER v7: User Manual/Tutorial. PRIMER-E, Plymouth, 18 (United Kingdom, 2015)

108.
Baselga, A. Partitioning the turnover and nestedness components of beta diversity. Glob. Ecol. Biogeogr. 19, 134–143 (2010).
Article  Google Scholar 

109.
Carvalho, J. C., Cardoso, P. & Gomes, P. Determining the relative roles of species replacement and species richness differences in generating beta-diversity patterns. Glob. Ecol. Biogeogr. 21, 760–771 (2012).
Article  Google Scholar 

110.
Qian, H., Ricklefs, R. E. & White, P. S. Beta diversity of angiosperms in temperate floras of eastern Asia and eastern North America. Ecol. Lett. 8, 15–22 (2005).
Article  Google Scholar  More

1.
Murchison, E. P. Clonally transmissible cancers in dogs and Tasmanian devils. Oncogene 27, S19–S30 (2008).
CAS  PubMed  Article  PubMed Central  Google Scholar 
2.
Metzger, M. J. et al. Widespread transmission of independent cancer lineages within multiple bivalve species. Nature 534, 705–709 (2016).
ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

3.
Storfer, A. et al. The devil is in the details: Genomics of transmissible cancers in Tasmanian devils. PLoS Pathog. 14, 1–7 (2018).
Article  CAS  Google Scholar 

4.
Nowinsky, M. A. Zur Frage über die Impfung der krebsigen Geschwülste. Zentralbl Med Wissensch. 14, 790–791 (1876).
Google Scholar 

5.
Murgia, C., Pritchard, J. K., Kim, S. Y., Fassati, A. & Weiss, R. A. Clonal origin and evolution of a transmissible cancer. Cell 126, 477–487 (2006).
CAS  PubMed  PubMed Central  Article  Google Scholar 

6.
Pearse, A. M. & Swift, K. Allograft theory: transmission of devil facial-tumour disease. Nature 439, 549 (2006).
ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

7.
Siddle, H. V. et al. Transmission of a fatal clonal tumor by biting occurs due to depleted MHC diversity in a threatened carnivorous marsupial. Proc. Natl. Acad. Sci. USA 104, 16221–16226 (2007).
ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

8.
Metzger, M. J. J., Reinisch, C., Sherry, J. & Goff, S. P. P. Horizontal transmission of clonal cancer cells causes leukemia in soft-shell clams. Cell 161, 255–263 (2015).
CAS  PubMed  PubMed Central  Article  Google Scholar 

9.
Riquet, F., Simon, A. & Bierne, N. Weird genotypes? Don’t discard them, transmissible cancer could be an explanation. Evol. Appl. 10, 140–145 (2017).
CAS  PubMed  Article  PubMed Central  Google Scholar 

10.
Yonemitsu, M. A. et al. A single clonal lineage of transmissible cancer identified in two marine mussel species in South America and Europe. Elife 8, 1–21 (2019).
Article  Google Scholar 

11.
Woods, G. M., Bruce Lyons, A. & Bettiol, S. S. A devil of a transmissible cancer. Trop. Med. Infect. Dis. 5, 1–10 (2020).
Google Scholar 

12.
Ganguly, B., Das, U. & Das, A. K. Canine transmissible venereal tumour: a review. Vet. Comp. Oncol. 14, 1–12 (2016).
CAS  PubMed  Article  Google Scholar 

13.
Paynter, A. N., Metzger, M. J., Sessa, J. A. & Siddall, M. E. Evidence of horizontal transmission of the cancer-associated Steamer retrotransposon among ecological cohort bivalve species. Dis. Aquat. Organ. https://doi.org/10.3354/dao03113 (2017).
Article  PubMed  Google Scholar 

14.
Barber, B. J. Neoplastic diseases of commercially important marine bivalves. Aquat. Living Resour. 17, 449–466 (2004).
Article  Google Scholar 

15.
Farley, C. A. Sarcomatoid proliferative disease in a wild population of blue mussels (Mytilus edulis). J. Natl. Cancer Inst. 43, 509–516 (1969).
CAS  PubMed  PubMed Central  Google Scholar 

16.
Sparks, A. K. Synopsis of Invertebrate Pathology Exclusive of Insects (Elsevier, 1985).
Google Scholar 

17.
Muttray, A. F. & Vassilenko, K. Mollusca: disseminated neoplasia in bivalves and the p53 protein family. Adv. Comp. Immunol. https://doi.org/10.1007/978-3-319-76768-0 (1969).
Article  Google Scholar 

18.
Bihari, N., Mičić, M., Batel, R. & Zahn, R. K. Flow cytometric detection of DNA cell cycle alterations in hemocytes of mussels (Mytilus galloprovincialis) off the Adriatic coast Croatia. Aquat. Toxicol. 64, 121–129 (2003).
CAS  PubMed  Article  PubMed Central  Google Scholar 

19.
Vassilenko, E. & Baldwin, S. A. Using flow cytometry to detect haemic neoplasia in mussels (Mytilus trossulus) from the Pacific Coast of Southern British Columbia Canada. J. Invertebr. Pathol. 117, 68–72 (2014).
PubMed  Article  PubMed Central  Google Scholar 

20.
Moore, J. D., Elston, R. A., Drum, A. S. & Wilkinson, M. T. Alternate pathogenesis of systemic neoplasia in the bivalve mollusc Mytilus. J. Invertebr. Pathol. 58, 231–243 (1991).
CAS  PubMed  Article  Google Scholar 

21.
Benabdelmouna, A., Saunier, A., Ledu, C., Travers, M. A. & Morga, B. Genomic abnormalities affecting mussels (Mytilus edulis-galloprovincialis) in France are related to ongoing neoplastic processes, evidenced by dual flow cytometry and cell monolayer analyses. J. Invertebr. Pathol. 157, 45–52 (2018).
Article  CAS  Google Scholar 

22.
Burioli, E. A. V. et al. Implementation of various approaches to study the prevalence, incidence and progression of disseminated neoplasia in mussel stocks. J. Invertebr. Pathol. 168, 107271 (2019).
CAS  PubMed  Article  Google Scholar 

23.
Moore, C. A., Beckmann, N. & Patricia Morse, M. Cytoskeletal structure of diseased and normal hemocytes of Mya arenaria. J. Invertebr. Pathol. 60, 141–147 (1992).
Article  Google Scholar 

24.
Carballal, M. J., Barber, B. J., Iglesias, D. & Villalba, A. Neoplastic diseases of marine bivalves. J. Invertebr. Pathol. https://doi.org/10.1016/j.jip.2015.06.004 (2015).
Article  PubMed  Google Scholar 

25.
Odintsova, N. A. Leukemia-like cancer in bivalves. Russ. J. Mar. Biol. 46, 59–67 (2020).
Article  Google Scholar 

26.
Smolarz, K., Renault, T. & Wołowicz, M. Ultrastructural study of neoplastic cells in Macoma balthica (Bivalvia) from the Gulf of Gdansk (Poland). J. Invertebr. Pathol. 92, 79–84 (2006).
PubMed  Article  Google Scholar 

27.
Carella, F. et al. Nuclear morphometry and ploidy of normal and neoplastic haemocytes in mussels. PLoS ONE 12, e0173219 (2017).
PubMed  PubMed Central  Article  CAS  Google Scholar 

28.
Smolowitz, R. M. & Reinisch, C. L. Indirect peroxidase staining using monoclonal antibodies specific for Mya arenaria neoplastic cells. J. Invertebr. Pathol. 48, 139–145 (1986).
CAS  PubMed  Article  Google Scholar 

29.
Carella, F., Figueras, A., Novoa, B. & De Vico, G. Cytomorphology and PCNA expression pattern in bivalves Mytilus galloprovincialis and Cerastoderma edule with haemic neoplasia. Dis. Aquat. Organ. 105, 81–87 (2013).
PubMed  Article  Google Scholar 

30.
McDonald, J. H., Seed, R. & Koehn, R. K. Allozymes and morphometric characters of three species of Mytilus in the Northern and Southern Hemispheres. Mar. Biol. 111, 323–333 (1991).
Article  Google Scholar 

31.
Larraín, M. A., Zbawicka, M., Araneda, C., Gardner, J. P. A. & Wenne, R. Native and invasive taxa on the Pacific coast of South America: impacts on aquaculture, traceability and biodiversity of blue mussels (Mytilus spp.). Evol. Appl. 11, 298–311 (2018).
Article  CAS  Google Scholar 

32.
Pye, R. J. et al. A second transmissible cancer in Tasmanian devils. Proc. Natl. Acad. Sci. USA 113, 374–379 (2016).
ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

33.
Strakova, A. et al. Mitochondrial genetic diversity, selection and recombination in a canine transmissible cancer. Elife 5, 1–25 (2016).
Article  Google Scholar 

34.
Rawson, P. D. & Harper, F. M. Colonization of the northwest Atlantic by the blue mussel, Mytilus trossulus postdates the last glacial maximum. Mar. Biol. 156, 1857–1868 (2009).
Article  Google Scholar 

35.
Wenne, R., Bach, L., Zbawicka, M., Strand, J. & McDonald, J. H. A first report on coexistence and hybridization of Mytilus trossulus and M. edulis mussels in Greenland. Polar Biol. 39, 343–355 (2016).
Article  Google Scholar 

36.
Laakkonen, H. M., Hardman, M., Strelkov, P. & Väinölä, R. Cycles of trans-Arctic dispersal and vicariance, and diversification of the amphi-boreal marine fauna. J. Evol. Biol. https://doi.org/10.1111/jeb.13674 (2020).
Article  PubMed  PubMed Central  Google Scholar 

37.
Zbawicka, M., Wenne, R. & Burzyński, A. Mitogenomics of recombinant mitochondrial genomes of Baltic Sea Mytilus mussels. Mol. Genet. Genom. 289, 1275–1287 (2014).
CAS  Article  Google Scholar 

38.
Śmietanka, B. & Burzyński, A. Disruption of doubly uniparental inheritance of mitochondrial DNA associated with hybridization area of European Mytilus edulis and Mytilus trossulus in Norway. Mar. Biol. https://doi.org/10.1007/s00227-017-3235-5 (2017).
Article  PubMed  PubMed Central  Google Scholar 

39.
Sunila, I. Histopathology of mussels (Mytilus edulis L.) from the Tvarminne area, the Gulf of Finland (Baltic Sea). Ann. Zool. Fennici 24, 55–69 (1987).
Google Scholar 

40.
Usheva, L. N. & Frolova, L. T. Neoplasia in the connective tissue tumor in the mussel Mytilus trossulus from a polluted region of Nakhodka Bay, the Sea of Japan. Ontogenez 31, 63–70 (2000).
CAS  PubMed  PubMed Central  Google Scholar 

41.
Maiorova, M. A. & Odintsova, N. A. β integrin-like protein-mediated adhesion and its disturbances during cell cultivation of the mussel Mytilus trossulus. Cell Tissue Res. 361, 581–592 (2015).
CAS  PubMed  Article  PubMed Central  Google Scholar 

42.
Marigomez, I., Lekube, X. & Cancio, I. Immunochemical localisation of proliferating cells in mussel digestive gland tissue. Histochem. J. 31, 781–788 (1999).
CAS  PubMed  Article  PubMed Central  Google Scholar 

43.
Maiorova, M. A. & Odintsova, N. A. Proliferative potential of larval cells of the mussel Mytilus trossulus and their capacity to differentiate into myogenic cells in culture. Russ. J. Mar. Biol. 42, 281–285 (2016).
Article  Google Scholar 

44.
Voronezhskaya, E. E., Nezlin, L. P., Odintsova, N. A., Plummer, J. T. & Croll, R. P. Neuronal development in larval mussel Mytilus trossulus (Mollusca: Bivalvia). Zoomorphology 127, 97–110 (2008).
Article  Google Scholar 

45.
Presa, P., Pérez, M., Diz, A. P., Perez, M. & Diz, A. P. Polymorphic microsatellite markers for blue mussels (Mytilus spp.). Conserv. Genet. 3, 441–443 (2002).
CAS  Article  Google Scholar 

46.
Zouros, E. Biparental inheritance through uniparental transmission: the doubly uniparental inheritance (DUI) of mitochondrial DNA. Evol. Biol. 40, 1–31 (2013).
Article  Google Scholar 

47.
Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547–1549 (2018).
CAS  PubMed  PubMed Central  Article  Google Scholar 

48.
Paabo, S., Irwin, M. & Wilson, C. DNA damage promotes jumping between templates during enzymatic amplification. J. Biol. Chem. 265, 4718–4721 (1990).
CAS  PubMed  Article  PubMed Central  Google Scholar 

49.
Bradley, R. D. & Hillis, D. A. Recombinant DNA sequences generated by PCR amplification. Mol. Biol. Evol. 14, 592–593 (1997).
CAS  PubMed  Article  PubMed Central  Google Scholar 

50.
Letunic, I. & Bork, P. Interactive Tree of Life (iTOL) v4: recent updates and new developments. Nucl. Acids Res. 47, 256–259 (2019).
Article  CAS  Google Scholar 

51.
Martin, D. P., Murrell, B., Golden, M., Khoosal, A. & Muhire, B. RDP4: detection and analysis of recombination patterns in virus genomes. Virus Evol. 1, 1–5 (2015).
Article  Google Scholar 

52.
Breton, S., Burger, G., Stewart, D. T. & Blier, P. U. Comparative analysis of gender-associated complete mitochondrial genomes in marine mussels (Mytilus spp.). Genetics 172, 1107–1119 (2006).
CAS  PubMed  PubMed Central  Article  Google Scholar 

53.
Marko, P. B. et al. The ‘Expansion-contraction’ model of Pleistocene biogeography: rocky shores suffer a sea change?. Mol. Ecol. 19, 146–169 (2010).
CAS  PubMed  Article  Google Scholar 

54.
Crego-Prieto, V., Juanes, F. & Garcia-Vazquez, E. Aquaculture and the spread of introduced mussel genes in British Columbia. Biol. Invasions https://doi.org/10.1007/s10530-015-0853-z (2015).
Article  Google Scholar 

55.
Chung, J. M. et al. Molecular phylogenetic study of bivalvia from four countries (China, Japan, Russia and Myanmar) using 3 types of primers. Korean J. Malacol. 35, 137–148 (2019).
Google Scholar 

56.
Layton, K. K. S., Martel, A. L., Hebert, P. D. N. & Layton, K. K. S. Patterns of DNA barcode variation in Canadian Marine molluscs. PLoS ONE 9, 1–9 (2014).
Article  Google Scholar 

57.
deWaard, J. R. et al. A reference library for Canadian invertebrates with 1.5 million barcodes, voucher specimens, and DNA samples. Sci. Data 6, 1–12 (2019).
Article  CAS  Google Scholar 

58.
Clement, M., Snell, Q., Walker, P., Posada, D. & Crandall, K. TCS: Estimating Gene Genealogies. Parallel Distrib. Process. Symp. Int. 2, 184 (2002).

59.
Leigh, J. W. & Bryant, D. POPART: full-feature software for haplotype network construction. Methods Ecol. Evol. 6, 1110–1116 (2015).
Article  Google Scholar 

60.
Kartavtsev, Y. P., Masalkova, N. A. & Katolikova, M. V. Genetic and morphometric variability in settlements of two mussel species (Mytilus ex. Gr. Edulis), Mytilus trossulus and Mytilus galloprovincialis, in the Northwestern Sea of Japan. J. Shellfish Res. 37, 103–119 (2018).
Article  Google Scholar 

61.
Larraín, M. A., González, P., Pérez, C. & Araneda, C. Comparison between single and multi-locus approaches for specimen identification in Mytilus mussels. Sci. Rep. 9, 1–13 (2019).
Article  CAS  Google Scholar 

62.
Inoue, K., Waite, J. H., Matsuoka, M., Odo, S. & Harayama, S. Interspecific variations in adhesive protein sequences of Mytilus edulis, M. galloprovincialis, and M. trossulus. Biol. Bull. 189, 370–375 (1995).
CAS  PubMed  Article  Google Scholar 

63.
Heath, D. D., Rawson, P. D. & Hilbish, T. J. PCR-based nuclear markers identify alien blue mussel Mytilus spp. genotypes on the west coast of Canada. Can. J. Fish. Aquat. Sci. 52, 2621–2627 (1995).
CAS  Article  Google Scholar 

64.
Rawson, P. D., Secor, C. L. & Hilbish, T. J. The effects of natural hybridization on the regulation of doubly uniparental mtDNA inheritance in blue mussels (Mytilus spp.). Genetics 144, 241–248 (1996).
CAS  PubMed  PubMed Central  Article  Google Scholar 

65.
Rawson, P. D. & Hilbish, T. J. Distribution of male and female mtDNA lineages in populations of blue mussels, Mytilus trossulus and M. galloprovincialis, along the Pacific coast of North America. Mar. Biol. 124, 245–250 (1995).
Article  Google Scholar 

66.
Cremonte, F., Vázquez, N. & Silva, M. R. Gonad atrophy caused by disseminated neoplasia in Mytilus chilensis cultured in the Beagle channel, Tierra Del Fuego Province Argentina. J. Shellfish Res. 30, 845–849 (2011).
Article  Google Scholar 

67.
Ciocan, C. & Sunila, I. Disseminated neoplasia in blue mussels, Mytilus galloprovincialis, from the Black Sea Romania. Mar. Pollut. Bull. 50, 1335–1339 (2005).
CAS  PubMed  Article  Google Scholar 

68.
Gombač, M., Sitar, R., Pogačnik, M., Arzul, I. & Jenčič, V. Haemocytic neoplasia in Mediterranean mussels (Mytilus galloprovincialis). Mar. Freshw. Behav. Physiol. 46, 135–143 (2013).
Article  Google Scholar 

69.
Villalba, A., Mourelle, S. G., Carballal, M. J. & López, C. Symbionts and diseases of farmed mussels Mytilus galloprovincialis throughout the culture process in the Rias of Galicia (NW Spain). Dis. Aquat. Organ. 31, 127–139 (1997).
Article  Google Scholar 

70.
Cremonte, F., Puebla, C., Tillería, J. & Videla, V. Estudio histopatológico del chorito Mytilus chilensis (Mytilidae) y del culengue Gari solida (Psammobiidae) en el sur de Chile. Lat. Am. J. Aquat. Res. 43, 248–254 (2015).
Article  Google Scholar 

71.
Vassilenko, E. I., Muttray, A. F., Schulte, P. M. & Baldwin, S. A. Variations in p53-like cDNA sequence are correlated with mussel haemic neoplasia: a potential molecular-level tool for biomonitoring. Mutat. Res. Genet. Toxicol. Environ. Mutagen. https://doi.org/10.1016/j.mrgentox.2010.06.001 (2010).
Article  Google Scholar 

72.
Caza, F., Bernet, E., Veyrier, F. J., Betoulle, S. & St-Pierre, Y. Hemocytes released in seawater act as Trojan horses for spreading of bacterial infections in mussels. Sci. Rep. 10, 1–12 (2020).
Article  CAS  Google Scholar 

73.
Rebbeck, C. A., Leroi, A. M. & Burt, A. Mitochondrial capture by a transmissible cancer. Science (80-) 331, 303 (2011).
ADS  CAS  Article  Google Scholar 

74.
Rawson, P. D. & Hilbish, T. J. Asymmetric introgression of mitochondrial DNA among European populations of Blue Mussels (Mytilus spp.). Evolution (N. Y.) 52, 100–108 (1998).
Google Scholar 

75.
Kijewski, A., Zbawicka, M., Väinölä, R. & Wenne, T. K. Introgression and mitochondrial DNA heteroplasmy in the Baltic populations of mussels Mytilus trossulus and M. edulis. Mar. Biol. https://doi.org/10.1007/s00227-006-0316-2 (2006).
Article  Google Scholar 

76.
Burzyński, A., Zbawicka, M., Skibinski, D. O. F. & Wenne, R. Evidence for recombination of mtDNA in the marine mussel Mytilus trossulus from the Baltic. Mol. Biol. Evol. 20, 388–392 (2003).
PubMed  Article  PubMed Central  Google Scholar 

77.
Burzynski, A., Zbawicka, M., Skibinski, D. O. F. & Wenne, R. Doubly uniparental inheritance is associated with high polymorphism for rearranged and recombinant control region haplotypes in Baltic Mytilus trossulus. Genetics 174, 1081–1094 (2006).
CAS  PubMed  PubMed Central  Article  Google Scholar 

78.
Stuckas, H., Stoof, K., Quesada, H. & Tiedemann, R. Evolutionary implications of discordant clines across the Baltic Mytilus hybrid zone (Mytilus edulis and Mytilus trossulus). Heredity (Edinb). 103, 146–156 (2009).
CAS  PubMed  Article  PubMed Central  Google Scholar 

79.
Cao, L., Kenchington, E. & Zouros, E. Differential segregation patterns of sperm mitochondria in embryos of the Blue Mussel (Mytilus edulis). Genetics https://doi.org/10.1534/genetics.166.2.883 (2004).
Article  PubMed  PubMed Central  Google Scholar  More

1.
Zhao, Y. Panax notoginseng (Burk.) F.H. Chen (Sanqi, Notoginseng) (eds. Liu, Y., Wang, Z. & Zhang, J.) 185–193 (Springer, 2015).
2.
Liao, P. et al. Stereoscopic cultivation of Panax notoginseng: A new approach to overcome the continuous cropping obstacle. Ind. Crop Prod. 126, 38–47 (2018).
CAS  Article  Google Scholar 

3.
Yang, M. et al. Autotoxic ginsenosides in the rhizosphere contribute to the replant failure of Panax notoginseng. PLoS ONE 10, e0118555 (2015).
PubMed  PubMed Central  Article  CAS  Google Scholar 

4.
Mazzola, M. & Manici, L. M. Apple replant disease: Role of microbial ecology in cause and control. Annu. Rev. Phytopathol. 50, 45–65 (2012).
CAS  PubMed  Article  PubMed Central  Google Scholar 

5.
Lovaisa, N. C. et al. Strawberry monocropping: Impacts on fruit yield and soil microorganisms. J. Soil Sci. Plant Nutr. 17, 868–883 (2017).
CAS  Article  Google Scholar 

6.
Petermann, J. S., Fergus, A. J. F., Turnbull, L. A. & Schmid, B. Janzen–Connell effects are widespread and strong enough to maintain diversity in grasslands. Ecology 89, 2399–2406 (2008).
PubMed  Article  PubMed Central  Google Scholar 

7.
Xia, P. G. et al. Optimal fertilizer application for Panax notoginseng and effect of soil water on root rot disease and saponin contents. J. Ginseng Res. 40, 38–46 (2016).
PubMed  Article  PubMed Central  Google Scholar 

8.
Dong, L., Xu, J., Feng, G., Li, X. & Chen, S. Soil bacterial and fungal community dynamics in relation to Panax notoginseng death rate in a continuous cropping system. Sci. Rep. 6, 31802 (2016).
ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

9.
Zhang, Y., Zheng, Y., Xia, P., Xun, L. & Liang, Z. Impact of continuous Panax notoginseng plantation on soil microbial and biochemical properties. Sci. Rep. 9, 13205 (2019).
ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

10.
Liu, D. H. et al. Study on dynamic change law of N, P and K in Panax notoginseng plant soils with different interval year. China J. Chin. Mater. Med. 39, 572–579 (2014).
ADS  Google Scholar 

11.
Vukicevich, E., Lowery, T., Bowen, P., Úrbez-Torres, J. R. & Hart, M. Cover crops to increase soil microbial diversity and mitigate decline in perennial agriculture. A review. Agron. Sustain. Dev. 36, 48 (2016).
Article  CAS  Google Scholar 

12.
Manici, L. M., Caputo, F. & Saccà, M. L. Secondary metabolites released into the rhizosphere by Fusarium oxysporum and Fusarium spp. as underestimated component of nonspecific replant disease. Plant Soil 415, 85–98 (2016).
Article  CAS  Google Scholar 

13.
Tan, Y. et al. Rhizospheric soil and root endogenous fungal diversity and composition in response to continuous Panax notoginseng cropping practices. Microbiol. Res. 194, 10–19 (2016).
PubMed  Article  PubMed Central  Google Scholar 

14.
Dumbrell, A. J., Nelson, M., Helgason, T., Dytham, C. & Fitter, A. H. Relative roles of niche and neutral processes in structuring a soil microbial community. ISME J. 4, 337–345 (2010).
PubMed  Article  PubMed Central  Google Scholar 

15.
Jeanbille, M. et al. Soil parameters drive the structure, diversity and metabolic potentials of the bacterial communities across temperate beech forest soil sequences. Microb. Ecol. 71, 482–493 (2016).
CAS  PubMed  Article  PubMed Central  Google Scholar 

16.
Wu, F. Y., Cui, X. M., Yang, Y. & Guan, H. L. Effects of soil pH values regulated by different fertilization on the disease incidence and growth of Panax notoginseng. J. Yunnan Univ. 39, 908–914 (2017).
Google Scholar 

17.
Wei, W., Yang, M., Liu, Y., Huang, H. & Zhu, S. Fertilizer N application rate impacts plant–soil feedback in a Sanqi production system. Sci. Total Environ. 633, 796–807 (2018).
ADS  CAS  PubMed  Article  Google Scholar 

18.
Killham, K. & Staddon, W. J. Bioindicators and sensors of soil health and the application of geostatistics (eds. Burns, R. G. & Dick, R. P.) 391–405 (Marcel Dekker, 2002).

19.
Kotroczó, Z. et al. Soil enzyme activity in response to long-term organic matter manipulation. Soil Biol. Biochem. 70, 237–243 (2014).
Article  CAS  Google Scholar 

20.
Sinsabaugh, R. L., Antibus, R. K. & Linkins, A. E. An enzymic approach to the analysis of microbial activity during plant litter decomposition. Agric. Ecosyst. Environ. 34, 43–54 (1991).
CAS  Article  Google Scholar 

21.
Li, W. H., Liu, Q. Z. & Chen, P. Effect of long-term continuous cropping of strawberry on soil bacterial community structure and diversity. J. Integr. Agric. 17, 2570–2582 (2018).
Article  Google Scholar 

22.
Sun, X. T. et al. Properties of soil physical–chemistry and activities of soil enzymes in context of continuous cropping obstacles for Panax notoginseng. Ecol. Environ. Sci. 24, 409–417 (2015).
Google Scholar 

23.
Sun, X. T. et al. The progress and prospect on consecutive monoculture problems of Panax notoginseng. Chin. J. Ecol. 34, 885–893 (2015).
Google Scholar 

24.
Tyler, G. & Falkengren-Grerup, U. Soil chemistry and plant performance-ecological consideration. Progr. Bot. 59, 634–658 (1998).
CAS  Article  Google Scholar 

25.
Utkhede, R. S. Soil sickness, replant problem or replant disease and its integrated control. Allelopathy J. 18, 23–38 (2006).
Google Scholar 

26.
Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. & Jarvis, A. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965–1978 (2005).
Article  Google Scholar 

27.
Lu, R. K. Analytical Method of Soil and Agricultural Chemistry 260–344 (China Agricultural Science and Technology Press, 2000).
Google Scholar 

28.
Guan, S. Soil Enzyme and Its Research Methods 22–36 (Agricultural Publisher, 1986).
Google Scholar 

29.
Zhang, Q. et al. Microcalorimetric study of the effects of long-term fertilization on soil microbial activity in a wheat field on the loess plateau. Ecotoxicology 23, 2035–2040 (2014).
CAS  PubMed  Article  PubMed Central  Google Scholar 

30.
Fellows, I. Deducer: A data analysis GUI for R. J. Stat. Softw. 49, 1–15 (2012).
Article  Google Scholar 

31.
Yang, M. et al. Steaming combined with biochar application eliminates negative plant-soil feedback for Sanqi cultivation. Soil Till. Res. 189, 189–198 (2019).
Article  Google Scholar 

32.
Tan, Y. et al. Diversity and composition of rhizospheric soil and root endogenous bacteria in Panax notoginseng during continuous cropping practices. J. Basic Microbiol. 57, 337–344 (2017).
CAS  PubMed  Article  PubMed Central  Google Scholar 

33.
Zhao, Y. M. et al. Role of phenolic acids from the rhizosphere soils of Panax notoginseng as a double-edge sword in the occurrence of root-rot disease. Molecules 23, 819 (2018).
PubMed Central  Article  CAS  Google Scholar 

34.
Wu, L. J., Guan, Y. M. & Liu, J. Y. Pollution-Free Cultivation of Panax notoginseng 69–79 (Chemical Industry Press, 2004).
Google Scholar 

35.
Du, C. Y., Zhang, N. M., Jiang, R., Wang, T. & Liu, Y. Evaluation of main soil nutrients characteristics for Panax notoginseng planting area of Yunnan. Southwest China J. Agric. Sci. 29, 599–605 (2016).
Google Scholar 

36.
Zhou, X. et al. Changes in rhizosphere soil microbial communities in a continuously monocropped cucumber (Cucumis sativus L.) system. Eur. J. Soil Biol. 60, 1–8 (2014).
CAS  Article  Google Scholar 

37.
Qin, S. H. et al. Breaking continuous potato cropping with legumes improves soil microbial communities, enzyme activities and tuber yield. PLoS ONE 12, e0175934 (2017).
PubMed  PubMed Central  Article  CAS  Google Scholar 

38.
Dou, F., Wright, A. L., Mylavarapu, R. S., Jiang, X. J. & Matocha, J. E. Soil enzyme activities and organic matter composition affected by 26 years of continuous cropping. Pedosphere 26, 618–625 (2016).
CAS  Article  Google Scholar 

39.
Wang, Y. et al. Effects of biochar on the growth of apple seedlings, soil enzyme activities and fungal communities in replant disease soil. Sci. Hortic. 256, 108641 (2019).
CAS  Article  Google Scholar 

40.
Adetunji, A. T., Lewu, F. B., Mulidzi, R. & Ncube, B. The biological activities of β-glucosidase, phosphatase and urease as soil quality indicators: A review. J. Soil Sci. Plant Nutr. 17, 794–807 (2017).
CAS  Article  Google Scholar 

41.
Strickland, M. S. & Rousk, J. Considering fungal:bacterial dominance in soils—Methods, controls, and ecosystem implications. Soil Biol. Biochem. 42, 1385–1395 (2010).
CAS  Article  Google Scholar 

42.
Malik, A. A. et al. Soil fungal:bacterial ratios are linked to altered carbon cycling. Front. Microbiol. 7, 1247 (2016).
PubMed  PubMed Central  Article  Google Scholar 

43.
Liu, X. et al. Soil fumigation and bio-organic fertilizer application promotes potato growth and affects soil bio-chemical properties in a continuous cropping system. Acta Pratacult. Sin. 24, 122–133 (2015).
Google Scholar 

44.
Liu, H. J. et al. Characteristics of soil microflora of Panax notoginseng in different continuous cropping years. Allelopathy J. 44, 145–158 (2018).
ADS  Article  Google Scholar 

45.
Singh, B. P., Cowi, A. L. & Chan, K. Y. Soil Health and Climate Change 69–85 (Springer, 2011).
Google Scholar 

46.
Turner, B. L. Variation in pH optima of hydrolytic enzyme activities in tropical rain forest soils. Appl. Environ. Microbiol. 76, 6485–6493 (2011).
Article  CAS  Google Scholar 

47.
Burns, R. G. et al. Soil enzymes in a changing environment: Current knowledge and future directions. Soil. Biol. Biochem. 58, 216–234 (2013).
CAS  Article  Google Scholar 

48.
Stark, S., Männistö, M. K. & Eskelinen, A. Nutrient availability and pH jointly constrain microbial extracellular enzyme activities in nutrient-poor tundra soils. Plant Soil 383, 373–385 (2014).
CAS  Article  Google Scholar 

49.
Hermans, S. M. et al. Bacteria as emerging indicators of soil condition. Appl. Environ. Microbiol. 83, e02826-e2916 (2017).
CAS  PubMed  Article  PubMed Central  Google Scholar 

50.
Dong, L. L. et al. Manipulation of microbial community in the rhizosphere alleviates the replanting issues in Panax ginseng. Soil. Biol. Biochem. 125, 64–74 (2018).
CAS  Article  Google Scholar 

51.
Li, X. et al. Effects of long-term continuous cropping on soil nematode community and soil condition associated with replant problem in strawberry habitat. Sci. Rep. 6, 30466 (2016).
ADS  CAS  PubMed  PubMed Central  Article  Google Scholar  More

Climate change has increased water temperature and altered wind-driven water movements in aquatic systems1,2. This applies not only to the mean conditions3,4, but also to the frequency of extreme events (i.e., near the upper ends of the range of observed values5,  > 80th percentile). For example, high air temperature or powerful winds5,6,7,8,9 has affected the behaviour of surface gravity waves10. Understanding the changes in wind and wave climate provides insight into the prediction and management of climate change impacts related to coastal dynamics, such as coastal erosion and sediment budgets, water motions, and biological responses6,11,12. Several studies on the impacts of climate change on oceanic waves12,13,14,15 have been undertaken, including a recent study16 that shows a 0.41% annual increase in global wave power (WP; the transport of energy by waves, which represents the temporal variations of energy transferred from the atmosphere to the ocean surface motion over cumulative periods of time16,17 (Eq. 2) due to stronger winds caused by increases in sea surface temperature. The oceanic wave climate also responds to global atmospheric phenomena (e.g., El Niño Southern Oscillation and the Atlantic Multidecadal Oscillation), in which sea surface temperature modifies wind patterns and storm cyclogenesis12,18,19,20. A systematic long-term assessment of climate warming impacts on waves in lakes remains to be undertaken, but should include winds, which are one of the principal sources of mechanical energy for lake circulation and interbasin coupling (e.g., exchange)21,22,23,24.
The Laurentian Great Lakes, which consist of lakes Superior, Michigan, Huron, Erie, and Ontario (Fig. 1a), are the largest group of freshwater lakes on Earth; they contain 21% of the world’s volume of fresh surface water. These lakes have been affected by climate change in several ways including increased surface water temperature, longer summer stratification related hypoxia (i.e., dissolved oxygen [DO] concentrations  0.05); all the black bars are significant (i.e., p  8 m s−1) from the south and southwest that are the common wind directions over the Great Lakes23, tilt the thermocline upward in the western and northern part of the central basin due to Ekman transport of surface water southward22,38,42,43,44,45. As this hypolimnetic water upwells into shallower depths it can be transported counter clockwise by the alongshore surface currents moving to the west32. If there is a calm period following the high winds, the upwelled water in the northwestern part of the central basin will flow southward because of the pressure gradient and also in a clockwise direction (to the west) because of the Coriolis effect, and so will intrude into the western basin (i.e., a geostrophic flow) opposite to the hydraulic flow from the Detroit River (Fig. 1c)22,32,46. This causes the rapid (on the order of hours) formation of a thermocline within the northeastern portion of the western basin (Pelee Passage) due to the intrusion of low temperature bottom water22,42, which can also be hypoxic22 or anoxic (i.e., DO (approx) 0) at the sediment surface22 and contain high soluble reactive phosphorus concentrations (SRP; 0.02–0.05 mg L−1)47,48,49. Low values of sediment oxygen uptake are observed during these events in the western basin due to stratification and weak bottom shear and turbulence, which results in thicker diffusive sublayer22.
Interbasin exchange has been observed in lakes with multiple basins elsewhere (e.g., Lake Geneva50, Nechako Reservoir51) as well as in the Great Lakes region (e.g., Muskegon Bay52, Green Bay53, Kempenfelt Bay54, Pere Marquette River55). In Lake Michigan, for example, high winds can lead to coastal upwelling into Muskegon Lake causing episodic hypoxia52. In case of Lake Erie, interbasin exchange was identified as the dominant cause (63%) of hypoxia in the northeastern portion of the western basin during biweekly fishing trawls in August over the past 30 years22. However, there are no long-term continuous water quality observations to assess the occurrence and historic trends in these hypoxic events. Extreme winds prevailing from upwelling favourable directions (i.e., from the south and southwest) can generate strong surface waves and water currents through momentum flux at the air–water interface. Therefore, WP can be used as an indicator or proxy (but not the cause) of interbasin exchange. Here, we examine the historical trends in water temperature, winds and resultant waves in the context of climate change in the summer in the Great Lakes (Fig. 1a) with an emphasis on the western basin of Lake Erie (Fig. 1b). We examine data for August, which is the month when hypoxia is most likely to occur in dimictic north temperate lakes before the fall turnover, and when large HAB have been observed in the western basin of Lake Erie. August is also the time when the spatial extent of hypoxia in the central basin is the largest and when the aforementioned upwelling into the western basin is likely to occur22,40,56. The data examined are from buoys with the longest historical records (Fig. 1a and Table S1). We examine winds from the south and southwest directions, which are the common wind directions over the Great Lakes during August, and which are favourable for upwelling into the western basin of Lake Erie. The results show that the WP in Great Lakes has increased in the past 40 years. A pattern in WP (a proxy for hypoxic upwelling events into the western basin of Lake Erie) has also increased in frequency over this time, which has implications for the water quality (e.g., dissolved oxygen and total phosphorus) of the lake. The increased frequency of interbasin upwelling was confirmed using historical records of lake bottom water temperature (LBT), as well as dissolved oxygen and total phosphorus concentrations. This is the first time that WP has been identified as an indicator of climate change-driven biogeochemical responses in lakes.
Long-term trends in WP and LST in the Great Lakes
First, we investigate the historical trends in average lake surface temperature (LST), wind, and waves in the Great Lakes during August. Results show that LST and LSTw (hereinafter subscript ”w” is used to denote the variables measured during upwelling favourable winds from 180° to 270°, clockwise from north) have both increased significantly (p  0.2% year−1) since 1980, although lower trends were observed in lake Erie and Michigan (Figs. S1–S5 ((a) and (b)) and Table S1). These changes in the LST correspond to a warming trend in air temperature (Tair); the average Tair over the Great Lakes increased significantly by ~ 0.4 (pm) 0.2 ((pm) standard error) oC decade−1 since 1980 (Fig. S6a,b). There was an associated significant increase in wind speed (W) over the Great Lakes during August (Ww) of ~ 0.4 (pm) 0.1 m s−1 decade−1 for winds from the south and southwest (Figs. S1–S5 ((c) and (d)) and Table S1). Consequently, the wind stress associated with wind from the south and southwest over the water surface of the Great Lakes (({tau }_{w}=0.0012{rho }_{air}{W}_{w}^{2}), where ({rho }_{air})=1.22 kg m−3 is the density of air57, and the wind speed is measured 10 m above the water) increased significantly by 0.006 (pm) 0.002 Pa decade−1 during August (3.0 (pm) 0.9% year−1; Figs. S1–S5 ((e) and (f)) and Table S1).
The effects of increased wind stress can also be seen in wave power, which is a function of the square of significant wave height (the mean value of the largest third of the wave heights during typically 1 h, SWH) and the wave period (({T}_{p}); i.e., (WP propto {{T}_{p} times SWH}^{2})); and changes in wind are reflected in wave power ((WP propto {W}^{2.4}) and (propto {W}^{5}) for developing and fully developed waves, respectively; see “Materials and methods”). The average SWH and SWHw in the Great Lakes during August have increased significantly by 0.03 (pm) 0.02 and 0.04 (pm) 0.03 m decade−1, respectively (i.e., ~ 1.0 (pm) 0.8% and ~ 1.7 (pm) 1.5% year−1, respectively), and this is largely driven by the increase in the frequency of extreme surface winds58 (Figs. S1–S5g and h; WP responds to changes in mean values, but it is more sensitive to extreme events because WP (propto { SWH}^{2})16). Consequently, the average WP and WPw in the Great Lakes during August have increased by ~ 0.04 (pm) 0.02 and ~ 0.06 (pm) 0.03 kW m−1 decade−1, respectively (i.e., ~ 1.0 (pm) 0.6% and ~ 2.0 (pm) 0.9% year−1, respectively; Fig. 2). In Lake Erie, WPw during August increased significantly by 0.02 (pm) 0.01 kW m−1 decade−1 (1.4 (pm) 0.2% year−1; Fig. 2 and Table S1; the increasing trend in WP = 0.02 (pm) 0.02 or 0.5 (pm) 0.1% was not statistically significant). It is relevant to note that these results are based on observations from a single buoy per lake; the one with the longest available data records (Fig. 1a and Table S2). However, the wind records and historical wave trends between buoys Sta. NDBC 45005 and Port Stanley in Lake Erie (Fig. 1a), which are ~ 130 km apart, are consistent based on the available records. Specifically, wind speed and direction in 2018 have Pearson correlation coefficients, r  > 0.6 (Fig. S7a,b, respectively); Ww and WPw are also correlated with r = 0.51 and 0.67, respectively, during August of 1990–2018 and the buoys show similar temporal increases in WPw (~ 0.025 (pm) 0.02 and 0.02 ± 0.01 kW m−1 decade−1 in Port Stanley and Sta. NDBC 45005, respectively). The trends in historical LSTw and WPw are related statistically (i.e., higher mutual information; Fig. S8) similar to the relationship described for global sea surface temperature and oceanic WP used as an indicator of climate change16.
Figure 2

Historical patterns in wave power in Great Lakes. 10 year moving average of wave power (WP) during the August (a) and during August with the wind from south and southwest and (WPw; b). The dashed lines show the linear regression (statistical results provided in Table S1).

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The long-term variations in WP and LST may be related to the global atmospheric phenomena. The LSTw anomaly in all the lakes show an increasing trend beginning in 1995 (Fig. S9a), which corresponds to the switch from the negative mode of the Atlantic Multidecadal Oscillation (AMO) to the positive mode (associated with increased tropical cyclone activity and stronger westerly winds) between the 1980s and the early 2000s (Fig. S9b)16. Both the WPw and LSTw anomaly are positively correlated with the AMO (r ~ 0.50 and ~ 0.55, respectively, since 1990). Similar to global oceanic wave power16, peaks in WPw in the Great Lakes are associated with strong El Niño years (i.e., Multivariate El Niño/Southern Oscillation (MEI) greater than 1.5; Fig. S9c,d), which can contribute to the enhanced wind energy due to increased cyclonic events16. MEI and WPw in Great Lakes are generally correlated by r  > 0.45 since 1990, however, the impacts of global atmospheric events on temperature and water dynamics of Great Lakes requires further study.
Episodic hypoxic upwelling events in the western basin of Lake Erie
We used historical records (Table S2) of long-term near-bottom water temperature (1998–2018) and dissolved oxygen (2007–2018) in the northeastern portion of the western basin of Lake Erie as well as wave observations in the western portion of the central basin (1980–2018 in Sta. NDBC 45005, Fig. 1) in August to determine the frequency of hypoxic upwelling events and the impacts of these events on the total phosphorus concentration in the northeast portion of the western basin. These analyses do not include the local hypoxia due to periods of calm and warm atmospheric conditions that may occur annually31 and, which are different than episodic upwelling events. Intrusion of cold hypoxic hypolimnetic water from the central basin into the western basin, following high winds from upwelling favourable directions, can cause a sudden drop (on the order of hours) in LBT and dissolved oxygen (DO) when the hypolimnetic water in the central basin is hypoxic22. The LBT time series in the western basin from 2017 to 2018 show that LBT decreased more than 3 °C in less than 12 h during upwelling events; e.g., 9–16, 18–22 and 26–31 August 2018 at Sta E (Fig. 3b) and 24–29 August 2017 at Leamington and Sta E (Fig. S10b). The records of LBT measured by the Ontario Ministry of Natural Resources and Forestry (MNRF) in August in Leamington Ontario between 1998 and 2018 detected 23 events of intrusion of cold water, which are consistent with upwelling (the blue symbols in Fig. 4a).
Figure 3

Wave power and bottom water temperature during August 2018 in the western basin of Lake Erie. (a) Time series of wave power (WP; black line), wave period (Tp; magenta), and significant wave height (SWH; blue) recorded at Sta. NDBC 45005. (b) Time series of dissolved oxygen (DO; red) and water temperature (LBT; blue dashed-line) in Sta. E at 1 m above the bed and bottom water temperature in Leamington (blue solid-line) in August 2018. The red triangles represent the observed hypoxic events in the western basin of Lake Erie. The wave power of the waves from south and southwest (i.e., favourable for upwelling) are positive preceding upwelling.

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Figure 4

Number of hypoxic upwelling events in the western basin. (a) The number of hypoxic upwelling events based on patterns in wave power at Sta. NDBC 45005 (dark grey: average WPw  > 0.44 kW m−1, light grey: 0.37  8 m s−1 from similar directions, which corresponds to the ~ 80th percentile of wind speeds and is greater than the sum of the average and standard deviation of the wind speed (~ 6 and 2 m s−1, respectively). This wind threshold is consistent with Rao et al.’s44 wind speed that led to upwelling, which resulted in a fish kill along the north shore of the central basin in 2012.
We used a least-square method to find a wave pattern (i.e., wave direction, duration, and power) that could be applied to predict the number of upwelling events that could be hypoxic between 1998 and 2018 based on LBT observations. A rapid decrease in the LBT at both Sta E and Leamington (12 km vs. 20 km from the Pelee Passage, respectively) occurred during events in which the average WP was  > 0.44 kW m−1 (i.e., 22–24 August 2017; Fig. S10a,b). The model predicted 25 upwelling events at Leamington (dark bars in Fig. 4a) of which 23 were observed (as stated above; no data were available for 2012; blue circles in Fig. 4a) for waves from south and southwest that lasted for at least 15 h with an average wave power greater than 0.37 kW m−1. Of the 23 observed events, the model predicted 21 events providing a root mean square error [RMSE] of 0.20 events. We validated the model predictions using the biweekly DO measurements from MNRF cruises between 2007 and 2018, which happened to sample 17 of the 23 observed events of low LBT. We note, however, that two hypoxic upwelling events were also recorded outside the study period, i.e., early September; this supports the study’s focus on August. Hypoxic conditions (DO  1.6 events year−1 in 2018 based on a 10-year moving average. Specifically, 21 of 49 (~ 43%) upwelling events in the last four decades have occurred in the past 10 years. Thirty-two of these were strong events with WP  > 0.44 kW m−1, 15 of which (~ 47%) occurred after 2009. Interestingly, this pattern in wave power (i.e., waves from south and southwest that last for  > 15 h with an average WP  > 0.37 kW m−1 from the historical data) was also observed in August 1980 (Fig. 4a), when the LBT dropped following rapid formation of a thermocline, which at the time was attributed to the upwelling of hypolimnetic water from the central basin40,42. These results indicate that an increase in extreme winds from south and southwest during August, over the last four decades, has resulted in more frequent upwelling from the central basin into the western basin and consequently a greater number of episodic hypoxic events in that part of Lake Erie.
The effect of upwelling on phosphorus concentrations was examined through an analysis of the water column-average total phosphorus (TP) observations from biweekly cruises conducted by the MNRF at station W5 (Fig. 1b). We examined the available data recorded between 15 July and 15 September from 2000 to 2018 (3–5 records year−1; 66 observations in total), which is a period in which linear patterns in TP vs. sampling date were not evident (p  >   > 0.05). The z-score (standard deviate) was determined for the data within a given year (({mathrm{Z}}_{mathrm{TP}}=left(mathrm{TP}-{mathrm{TP}}_{mathrm{mean}}right)/mathrm{SD}), where ({mathrm{TP}}_{mathrm{mean}}) is the annual average of TP and SD is the standard deviation). Positive ({mathrm{Z}}_{mathrm{TP}}) values (i.e., (mathrm{TP} >{mathrm{TP}}_{mathrm{mean}})) were observed in 11 cases in which the sampling occurred  1) observed during 5 August–8 September sampling (black solid circles in Fig. 4b). Statistical comparison revealed that the average ({mathrm{Z}}_{mathrm{TP}}) was significantly higher during upwelling vs. non-upwelling samples (i.e., 0.95 ± 0.18, n = 11 vs. − 0.26 ± 0.12, n = 25; ANOVA F1,34 = 29.64, p  More

1.
Dujardin, J. P. Aporte de la genetica poblacional al control y vigilancia de vectores de la enfermedad de Chagas. In Curso Posgrado Genética Poblacional de Triatomineos Aplicada al Control Vectorial de la Enfermedad de Chagas (ed. Guhl, F.) 13–15 (Corcas Editores Ltda, 1997).
Google Scholar 
2.
Pires, H. H. R., Barbosa, S. E., Margonari, C., Jurberg, J. & Diotaiuti, L. Variations of the external male genitalia in three populations of Triatoma infestans Klug, 1834. Minist. Saúde 93(4), 479–483 (1998).
CAS  Google Scholar 

3.
Bambou, A. E. et al. Comparing genetic diversity of Sitophilus zeamais(Motchulsky) populations sampled in several agro-ecological areas between Central African Republic and Senegal. South Asian J. Exp. Biol. 4(4), 172–182 (2014).
Google Scholar 

4.
Baldwin, J. D. & Dingle, H. Geographic variation in the effects of temperature on life-history traits in the large milkweed bug Oncopeltus fasciatus. Oecologia 69, 64–71 (1986).
ADS  Article  Google Scholar 

5.
Blanckenhorn, W. U. Altitudinal life history variation in the dung flies Scathophaga stercoraria and Sepsis cynipsea. Oecologia 109, 342–352 (1997).
ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

6.
Ikten, C., Skoda, S. R., Hunt, T. E., Molina-Ochoa, J. & Foster, J. E. Genetic variation and inheritance of diapause induction in two distinct voltine ecotypes of Ostrinia nubilalis (Lepidoptera: Crambidae). Ann. Entomol. Soc. Am. 104, 567–575 (2011).
Article  Google Scholar 

7.
Dhillon, M. K., Hasan, F., Tanwar, A. K. & Bhadauriya, A. P. S. Effects of thermo-photoperiod on induction and termination of hibernation in Chilo partellus (Swinhoe). Bull. Entomol. Res. 107, 294–302 (2017).
CAS  PubMed  Article  PubMed Central  Google Scholar 

8.
Sharma, H. C. Host plant resistance to insects in sorghum and its role in integrated pest management. Crop Prot. 12, 11–34 (1993).
Article  Google Scholar 

9.
Dhillon, M. K., Hasan, F., Tanwar, A. K. & Bhadauriya, A. P. S. Factors responsible for aestivation in spotted stem borer, Chilo partellus (Swinhoe). J. Exp. Zool. A 331, 326–340 (2019).
Article  Google Scholar 

10.
Dhillon, M. K. & Hasan, F. Consequences of diapause on post-diapause development, reproductive physiology and population growth of Chilo partellus (Swinhoe). Physiol. Entomol. 43, 196–206 (2018).
CAS  Article  Google Scholar 

11.
Dhillon, M. K., Tanwar, A. K. & Hasan, F. Fitness consequences of delayed mating on reproductive performance of Chilo partellus (Swinhoe). J. Exp. Zool. A 331, 161–167 (2019).
Article  Google Scholar 

12.
Dhillon, M. K. et al. Genetic regulation of diapause and associated traits in Chilo partellus (Swinhoe). Sci. Rep. 10, 1793 (2020).
ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

13.
Chown, S. L. & Terblanche, J. S. Physiological diversity in insects: Ecological and evolutionary contexts. Adv. Insect Physiol. 33, 50–152 (2006).
Article  Google Scholar 

14.
Sezonlin, M. et al. Phylogeography and population genetics of the maize stalk borer Busseola fusca (Lepidoptera, Noctuidae) in sub-Saharan Africa. Mol. Ecol. 15(2), 407–420 (2006).
CAS  PubMed  Article  Google Scholar 

15.
Rowntree, J. K., Cameron, D. D. & Preziosi, R. F. Genetic variation changes the interactions between the parasitic plant-ecosystem engineer Rhinanthus and its hosts. Philos. Trans. R. Soc. B 366, 1380–1388 (2011).
Article  Google Scholar 

16.
Giron, D. et al. Promises and challenges in insect–plant interactions. Entomol. Exp. Appl. 166(5), 319–343 (2018).
Article  Google Scholar 

17.
Williams, R. S. & Howells, J. M. Effects of intraspecific genetic variation and prior herbivory in an old-field plant on the abundance of the specialist aphid Uroleucon nigrotuberculatum (Hemiptera: Aphididae). Environ. Entomol. 47, 422–431 (2018).
CAS  PubMed  Article  PubMed Central  Google Scholar 

18.
Matsubayashi, K. W., Ohshima, I. & Nosil, P. Ecological speciation in phytophagous insects. Entomol. Exp. Appl. 134, 1–27 (2010).
Article  Google Scholar 

19.
Feder, J. L. et al. Allopatric genetic origins for sympatric host-plant shifts and race formation in Rhagoletis. Proc. Natl Acad. Sci USA 100, 10314–10319 (2003).
ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

20.
Althoff, M. D. & Pellmyr, O. Examining genetic structure in bogus yucca moth: A sequential approach to phylogeography. Evolution 56, 1632–1643 (2002).
PubMed  Article  Google Scholar 

21.
Knowles, L. L. & Maddison, W. P. Statistical phylogeography. Mol. Ecol. 11, 2623–2635 (2002).
PubMed  Article  Google Scholar 

22.
Templeton, A. R. Statistical phylogeography: Methods of evaluating and minimizing inference errors. Mol. Ecol. 13, 789–809 (2004).
PubMed  Article  Google Scholar 

23.
Thomas, Y., Bethenod, M. T., Pelozuelo, L., Frérot, B. & Bourguet, D. Genetic isolation between two sympatric host-plant races of the European corn borer, Ostrinia nubilalis Hübner. I. Sex pheromone, moth emergence timing, and parasitism. Evolution 57, 261–273 (2003).
PubMed  Google Scholar 

24.
Sharma, H. C., Taneja, S. L., Kameswara Rao, N. & Prasada Rao, K. E. Evaluation of sorghum germplasm for resistance to insect pests. Inf. Bull. 63, 177 (2003).
Google Scholar 

25.
Sharma, H. C., Dhillon, M. K., Pampapathy, G. & Reddy, B. V. S. Inheritance of resistance to spotted stem borer, Chilo partellus in sorghum, Sorghum bicolor. Euphytica 156, 117–128 (2007).
Article  Google Scholar 

26.
Kanta, U., Dhillon, B. S. & Sekhon, S. S. Evaluation and development of maize germplasm for resistance to spotted stem borer. In Insect Resistant Maize: Recent Advances and Utilization (ed. Mihm, J. A.) 246–254 (Proceedings of an International Symposium CIMMYT, 1997).
Google Scholar 

27.
Rakshit, S. et al. Catalogue of Indian maize inbred lines. Tech. Bull. 3, 40 (2008).
Google Scholar 

28.
Agrawal, A. A. Phenotypic plasticity in the interactions and evolution of species. Science 294, 321–326 (2001).
ADS  CAS  PubMed  Article  Google Scholar 

29.
Stireman, J. O. III., Nason, J. D. & Heard, S. B. Host-associated genetic differentiation in phytophagous insects: general phenomenon or isolated exceptions? Evidence from a goldenrod-insect community. Evolution 59, 2573–2587 (2005).
CAS  PubMed  Article  Google Scholar 

30.
Zytynska, S. E. & Preziosi, R. F. Genetic interactions influence host preference and performance in a plant-insect system. Evol. Ecol. 25, 1321–1333 (2011).
Article  Google Scholar 

31.
Zytynska, S. E. & Preziosi, R. F. Host preference of plant genotypes is altered by intraspecific competition in a phytophagous insect. Arthropod-Plant Interact. 7, 349–357 (2013).
Article  Google Scholar 

32.
Sharma, H. C. Biotechnological Approaches for Pest Management and Ecological Sustainability (CRC Press, 2009).
Google Scholar 

33.
Sharma, H. C. & Dhillon, M. K. Climate change effects on arthropod diversity and its implications for pest management and sustainable crop production. In Agroclimatology: Linking Agriculture to Climate (eds Hatfield, J. L. et al.) 595–619 (Crop Science Society of America and Soil Science Society of America Inc, Madison, WI, 2020).
Google Scholar 

34.
Smith, C. M. Plant Resistance to Arthropods: Molecular and Conventional Approaches (Springer, 2005).
Google Scholar 

35.
Dhillon, M. K. & Sharma, H. C. Paradigm shifts in research on host plant resistance to insect pests. Indian J. Plant Protect. 40(1), 1–11 (2012).
Google Scholar 

36.
Funk, D. J. Isolating a role for natural selection in speciation: Host adaptation and sexual isolation in Neochlamisus bebbianae leaf beetles. Evolution 52, 1744–1759 (1998).
PubMed  Article  PubMed Central  Google Scholar 

37.
Dres, M. & Mallet, J. Host races in plant-feeding insects and their importance in sympatric speciation. Philos. Trans. R. Soc. B 357, 471–492 (2002).
Article  Google Scholar 

38.
Rundle, H. D. & Nosil, P. Ecological speciation. Ecol. Lett. 8, 336–352 (2005).
Article  Google Scholar 

39.
Schluter, D. Evidence for ecological speciation and its alternative. Science 323, 737–741 (2009).
ADS  CAS  PubMed  Article  Google Scholar 

40.
Ishiguro, N. & Tsuchida, K. Polymorphic microsatellite loci for the rice stem borer, Chilo suppressalis (Walker) (Lepidoptera: Crambidae). Appl. Entomol. Zool. 41, 565–568 (2006).
CAS  Article  Google Scholar 

41.
Mukhopadhyay, J., Ghosh, K., Rangel, E. F. & Munstermann, L. E. Genetic variability in biochemical characters of Brazilian field populations of the Leishmania vector, Lutzomyia longipalpis (Diptera: Psychodidae). Am. J. Trop. Med. Hyg. 59(6), 893–901 (1998).
CAS  PubMed  Article  PubMed Central  Google Scholar 

42.
Vijaya Lakshmi, P., Amudhan, S., Bindu, K. H., Cheralu, C. & Bentur, J. S. A new biotype of the Asian rice gall midge Orseolia oryzae (Diptera: Cecidomyiidae) characterized from the Warangal population in Andhra Pradesh, India. Int. J. Trop. Insect Sci. 26, 207–211 (2006).
Google Scholar 

43.
Himabindu, K., Suneetha, K., Sama, V. S. A. K. & Bentur, J. S. A new rice gall midge resistance gene in the breeding line CR57-MR1523, mapping with flanking markers and development of NILs. Euphytica 174, 179–187 (2010).
CAS  Article  Google Scholar 

44.
Ratcliffe, R. H. et al. Biotype composition of Hessian fly (Diptera: Cecidomyiidae) populations from the Southeastern, Midwestern, and Northwestern United States and virulence to resistance genes in wheat. J. Econ. Entomol. 93(4), 1319–1328 (2000).
CAS  PubMed  Article  PubMed Central  Google Scholar 

45.
Zhou, H. et al. Genetic analysis and fine mapping of the gall midge resistance gene Gm5 in rice (Oryza sativa L.). Theor. Appl. Genet. 133, 2021–2033 (2020).
CAS  PubMed  Article  PubMed Central  Google Scholar 

46.
Dhillon, M. K. & Kumar, S. Amino acid profiling of Sorghum bicolor vis-à-vis Chilo partellus (Swinhoe) for biochemical interactions and plant resistance. Arthropod-Plant Interact. 11, 537–550 (2017).
Article  Google Scholar 

47.
Dhillon, M. K. & Kumar, S. Lipophilic profiling of Sorghum bicolor (L.) seedlings vis-à-vis Chilo partellus (Swinhoe) larvae reveals involvement of biomarkers in sorghum-stem borer interactions. Indian J. Exp. Biol. 58, 95–108 (2020).
CAS  Google Scholar 

48.
Atray, I., Bentur, J. S. & Nair, S. The Asian rice gall midge (Orseolia oryzae) mitogenome has evolved novel gene boundaries and tandem repeats that distinguish its biotypes. PLoS ONE 10(7), e0134625 (2015).
PubMed  PubMed Central  Article  CAS  Google Scholar 

49.
Fujita, D., Kohli, A. & Horgan, F. G. Rice resistance to planthoppers and leafhoppers. Crit. Rev. Plant Sci. 32, 162–191 (2013).
CAS  Article  Google Scholar 

50.
Diehl, R. S. & Bush, G. L. An evolutionary and applied perspective of insect biotypes. Annu. Rev. Entomol. 29, 471–504 (1984).
Article  Google Scholar 

51.
Claridge, M. F. & Den Hollander, J. A biotype concept and its application to insect pests of agriculture. Crop Prot. 2(1), 85–95 (1983).
Article  Google Scholar 

52.
Downie, D. A. Baubles, bangles, and biotypes: A critical review of the use and abuse of the biotype concept. J. Insect Sci. 10, 176 (2010).
CAS  PubMed  PubMed Central  Article  Google Scholar 

53.
Perring, T. M. The Bemisia tabaci species complex. Crop Prot. 20, 725–737 (2001).
Article  Google Scholar 

54.
Wenger, J. A. & Michel, A. P. Implementing an evolutionary framework for understanding genetic relationships of phenotypically defined insect biotypes in the invasive soybean aphid (Aphis glycines). Evol. Appl. 6(7), 1041–1053 (2013).
PubMed  PubMed Central  Article  Google Scholar 

55.
Sharma, H. C., Taneja, S. L., Leuschner, K. & Nwanze, K. F. Techniques to screen sorghum for resistance to insect pests. Inf. Bull. 32, 48 (1992).
Google Scholar 

56.
Kumar, S. & Dhillon, M. K. Lipophilic metabolite profiling of maize and sorghum seeds and seedlings, and their pest spotted stem borer larvae: A standardized GC-MS based approach. Indian J. Exp. Biol. 53, 170–176 (2015).
PubMed  Google Scholar 

57.
Dhillon, M. K., Kumar, S. & Gujar, G. T. A common HPLC-PDA method for amino acid analysis in insects and plants. Indian J. Exp. Biol. 52, 73–79 (2014).
CAS  PubMed  Google Scholar  More

Physicochemical and chemical properties of soils and BioC
The physicochemical and chemical characteristics of the soils and BioC, as well as selected chemical properties of the HAs isolated from the soil and BioC are shown in Table 1.
Table 1 Physicochemical and chemical characteristics of soils, BioC and isolated HAs.
Full size table

The properties of soils and BioC, such as the d, Corg, A, pH, and Q, were presented in detail previously4. Briefly, soils were characterised by a typical d value for mineral soils ≈ 2.60 g cm−3, and by a relatively low content of Corg and a high content of A. The pH of the soils was weakly acidic. The examined soils were characterised by low Q values, indicating a low content of organic structures dissociating to the negative surface charge (mainly carboxylic and phenolic groups). The HAs obtained from fallow and grassland were characterised by high QHA values (about 50 times higher in comparison with the Q values of fallow and grassland). The d value of BioC was typical for organic materials (1.46 g cm−3), moreover, the BioC contained a high content of OM, which was expressed as Corg. The pH of BioC was alkaline. This material was also characterised by a high Q value, which indicated its favourable sorption properties.
The results of our studies showed that the E2/6 values were similar for the HAs originated from the two studied soils, suggesting a similar ratio of lignin-type compounds resistant to humification to the structures with a high humification degree. The ΔlgK reached values of 0.83 and 0.86 for HAs isolated from grassland and fallow, respectively, indicating a low degree of HA humification (Kumada’s classification for low humification degree of HAs: ΔlgK = 0.8–1.1)33. Slightly higher ΔlgK values obtained for the grassland HAs compared with the fallow suggested a higher content of less humified compounds, such as cellulose, hemicellulose, and lignin34.
The ΔlgK of HAs isolated from BioC reached a value of 0.54, suggesting the presence of highly humified compounds, in comparison with soil HAs (Kumada’s classification for high humification degree of HAs: ΔlgK  8.0, above which the OH groups are deprotonated26, therefore we only report results in this pH range. Changes in the QHA values as a function of pH (Fig. 4A–D) were monotonic; these values increased towards an alkaline pH, which resulted from the fact that other fractions of functional groups dissociated successively at increasing pH values. Generally, in the first month of the experiment, the highest QHA values were observed for HAs obtained from fallow and grassland with the lowest BioC dose (Fig. 4A,C). This fact indicated that these HAs had the best sorption properties. In the last month of the experiment, the QHA values changed in an ambiguous way. The QHA at pH 9.0 values of HAs isolated from pure BioC were lower than those obtained from the soil, and moreover, BioC did not have an obvious effect on the QHA values of the soil HAs. Previous studies4 on impact of BioC on the physicochemical properties of Haplic Luvisol under different land uses, showed that BioC added to soil caused a significant increase in Q values in the last year of the experiment. Thus, we can conclude that BioC introduced OM with a variable surface charge but did not affect the soil’s QHA. It is possible that the BioC doses used in our experiment were insufficient to raise the QHA values.
Figure 4

Dependence of surface negative charge (QHA) on pH of the HAs solution. HAs obtained from fallow (A,B) and grassland (C,D) amended with BioC in 1st and 28th month of field experiment, as well as HAs obtained from BioC.

Full size image

Influence of BioC amendment on structure and chemical properties of HAs in fallow and grassland: spectroscopic approach
The analyses of the HAs isolated from fallow and grassland amended with BioC showed changes in the structural properties of these compounds. The E2/6 parameter estimated from UV–Vis data was changing both under the influence of different BioC doses and during the 3 years of the experiment. However, it should be assumed that the observed changes were of a different nature for fallow (Fig. 5A) and for grassland (Fig. 5B), due to varied trends in the activity of BioC on the analysed soils.
Figure 5

Changes in E2/6 values obtained for HAs of fallow (A) and grassland (B) amended with BioC (0, 1, 2, 3 kg m−2) as a function of time. Average values from 3 replicates in each term, ± standard deviation. Other letter designations indicate significant differences between values at α  More

1.
Bennett, M. R. & Morse, S. A. Human Footprints: Fossilised Locomotion? (Springer International Publishing, Berlin, 2014).
Google Scholar 
2.
Leakey, M. D. & Hay, R. L. Pliocene footprints in the Laetolil Beds at Laetoli, northern Tanzania. Nature 278, 317–323 (1979).
ADS  Article  Google Scholar 

3.
Mietto, P., Avanzini, M. & Rolandi, G. Palaeontology: Human footprints in Pleistocene volcanic ash. Nature 422, 133 (2003).
ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

4.
Ashton, N. et al. Hominin footprints from early Pleistocene deposits at Happisburgh, UK. PLoS ONE 9, e88329 (2014).
ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

5.
Duveau, J. et al. The composition of a Neandertal social group revealed by the hominin footprints at Le Rozel (Normandy, France). PNAS 116, 19409–19414 (2019).
CAS  PubMed  Article  PubMed Central  Google Scholar 

6.
Masao, F. T. et al. New footprints from Laetoli (Tanzania) provide evidence for marked body size variation in early hominins. eLife 5, e19568 (2016).
PubMed  PubMed Central  Article  Google Scholar 

7.
Altamura, F. et al. Archaeology and ichnology at Gombore II-2, Melka Kunture, Ethiopia: Everyday life of a mixed-age hominin group 700,000 years ago. Sci. Rep. 8, 2815 (2018).
ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

8.
Bustos, D. et al. Footprints preserve terminal Pleistocene hunt? Human-sloth interactions in North America. Sci. Adv. 4, eaar7621 (2018).
ADS  PubMed  PubMed Central  Article  Google Scholar 

9.
Stewart, M. et al. Human footprints provide snapshot of last interglacial ecology in the Arabian interior. Sci. Adv. 6, eaba8940 (2020).
ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

10.
Barton, C. M. Stone tools and paleolithic settlement in the Iberian Peninsula. Proc. Prehist. Soc. 56, 15–32 (1990).
Article  Google Scholar 

11.
Garralda, M. D. The Neandertals from the Iberian Peninsula. MUNIBE 57, 289–314 (2005).
Google Scholar 

12.
Ruiz, M. N. et al. Last Neandertal occupations at Central Iberia: The lithic industry of Jarama VI rock shelter (Valdesotos, Guadalajara, Spain). Archaeol. Anthropol. Sci. 12, 45 (2020).
Article  Google Scholar 

13.
Muñiz, F. et al. Following the last Neandertals: Mammal tracks in Late Pleistocene coastal dunes of Gibraltar (S Iberian Peninsula). Quat. Sci. Rev. 217, 297–309 (2019).
ADS  Article  Google Scholar 

14.
Neto de Carvalho, C. et al. First vertebrate tracks and palaeoenvironment in a MIS-5 context in the Doñana National Park (Huelva, SW Spain). Quat. Sci. Rev. 243, 106508 (2020).
Article  Google Scholar 

15.
Neto de Carvalho, C. et al. Paleoecological implications of large-sized wild boar tracks recorded during the last interglacial (Mis 5) at Huelva (Sw Spain). Palaios 35, 512–523 (2020).
ADS  Article  Google Scholar 

16.
Rodríguez-Ramírez, A. et al. The role of neo-tectonics in the sedimentary infilling and geomorphological evolution of the Guadalquivir estuary (Gulf of Cadiz, SW Spain) during the Holocene. Geomorphology 219, 126–140 (2014).
ADS  Article  Google Scholar 

17.
Rodríguez-Rámirez, A. Geomorfología del Parque Nacional de Doñana y su Entorno. (ed Organismo Autónomo Parques Nacionales) (Ministerio de Medio Ambiente, Madrid, 1998).

18.
Pérez Muñoz, A. B. et al. Parque Nacional de Doñana. Guía Geológica. (ed Rodríguez Fernández, R.) (Instituto Geológico y Minero de España & Organismo Autónomo Parques Nacionales, Madrid, 2020).

19.
Instituto Hidrográfico de la Marina. Derrotero N° 2-Tomo 2 (Costas de Portugal y SO de España, Cádiz, 1992).
Google Scholar 

20.
Rodríguez-Ramírez, A. et al. Analysis of the recent storm record in the southwestern spanish coast: Implications for littoral management. Sci. Total Environ. 303, 189–201 (2003).
ADS  PubMed  Article  CAS  PubMed Central  Google Scholar 

21.
Gibbard, P. L., Head, M. J., Walker, M. J. C. & The Subcommission on Quaternary Stratigraphy. Formal ratification of the Quaternary System/Period and the Pleistocene Series/Epoch with a base at 2.58 Ma. J. Quat. Sci. 25, 96–102 (2010).
Article  Google Scholar 

22.
Zazo, C. et al. Landscape evolution and geodynamic controls in the Gulf of Cadiz (Huelva coast, SW Spain) during the Late Quaternary. Geomorphology 68, 269–290 (2005).
ADS  Article  Google Scholar 

23.
Duveau, J. Les empreintes de pieds du Rozel (Manche). Instantanés de groupes humains au Pléistocène supérieur. Approche combinée morphométrique et expérimentale. (Ph. D. dissertation. Muséum national d’Histoire naturelle, Paris, 2020).

24.
Manolis, S., Aiello, L., Henessy, R., Kyparissi-Apostolika, N. Middle Palaeolithic Footprints from Theopetra Cave (Thessaly, Greece) (ed Kyparissi-Apostolika, N.) 87–93 (Greek Ministry of Culture and Institute for Aegean Prehistory, Athens, 2000).

25.
Onac, B. P. et al. U-Th ages constraining the Neanderthal footprint at Vârtop Cave, Romania. Quat. Sci. Rev. 24, 1151–1157 (2005).
ADS  Article  Google Scholar 

26.
Duveau, J., Berillon, G., Verna, C. 11-On the tracks of Neandertals: The ichnological assemblage from Le Rozel (Normandy, France). (eds Pastoors, A. & Lenssen-Erz, T.) (Springer Nature, in Press).

27.
Citton, P., Romano, M., Salvador, I. & Avanzini, M. Reviewing the upper Pleistocene human footprints from the ‘Sala dei Misteri’in the Grotta della Basura (Toirano, northern Italy) cave: An integrated morphometric and morpho-classificatory approach. Quat. Sci. Rev. 169, 50–64 (2017).
ADS  Article  Google Scholar 

28.
Helm, C. W. et al. A New Pleistocene Hominin Tracksite from the Cape South Coast, South Africa. Sci. Rep. 8, 3772 (2018).
ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

29.
Dingwall, H. L., Hatala, K. G., Wunderlich, R. E. & Richmond, B. G. Hominin stature, body mass, and walking speed estimates based on 1.5 million-year-old fossil footprints at Ileret, Kenya. J. Hum. Evol. 64, 556–568 (2013).
PubMed  Article  PubMed Central  Google Scholar 

30.
Krishan, K. Estimation of stature from footprint and foot outline dimensions in Gujjars of North India. Forensic Sci. Int. 175, 93–101 (2008).
PubMed  Article  PubMed Central  Google Scholar 

31.
Fawzy, I. A. & Kamal, N. N. Stature and body weight estimation from various footprint measurements among Egyptian population. J. Forensic Sci. 55, 884–888 (2010).
PubMed  Article  PubMed Central  Google Scholar 

32.
Reel, S., Rouse, S., Obe, W. V. & Doherty, P. Estimation of stature from static and dynamic footprints. Forensic Sci. Int. 219, 283-e1 (2012).
PubMed  Article  PubMed Central  Google Scholar 

33.
Hemy, N., Flavel, A., Ishak, N. I. & Franklin, D. Sex estimation using anthropometry of feet and footprints in a Western Australian population. Forensic Sci. Int. 231, 402-e1 (2013).
PubMed  Article  PubMed Central  Google Scholar 

34.
Aiello, L. & Dean, C. An Introduction to Human Evolutionary Anatomy (Academic Press Inc., London, 1990).
Google Scholar 

35.
Klenerman, L. & Wood, B. The Human Foot: A Companion to Clinical Studies (Springer, London, 2006).
Google Scholar 

36.
Elftman, H. & Manter, J. Chimpanzee and human feet in bipedal walking. Am. J. Phys. Anthropol. 20, 69–79 (1935).
Article  Google Scholar 

37.
Alexander, R. M. Principles of Animal Locomotion (Princeton University Press, Princeton, 2003).
Google Scholar 

38.
Ruff, C. B., Trinkaus, E. & Holliday, T. W. Body mass and encephalization in Pleistocene Homo. Nature 387, 173 (1997).
ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

39.
Carretero, J. M. et al. Stature estimation from complete long bones in the Middle Pleistocene humans from the Sima de los Huesos, Sierra de Atapuerca (Spain). J. Hum. Evol. 62, 242–255 (2012).
PubMed  Article  PubMed Central  Google Scholar 

40.
Benazzi, S. et al. Early dispersal of modern humans in Europe and implications for Neandertal behaviour. Nature 479, 525–528 (2011).
ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

41.
Hublin, J. J. The modern human colonization of western Eurasia: When and where?. Quat. Sci. Rev. 118, 194–210 (2015).
ADS  Article  Google Scholar 

42.
Karavanić, I. et al. Paleolithic hominins and settlement in Croatia from MIS 6 to MIS 3: Research history and current interpretations. Quat. Int. 494, 152–166 (2018).
Article  Google Scholar 

43.
Vallespi, E., Alvarez, G., Perez Sindreu, F. & Rufete, P. Nuevas atribuciones onubenses al Paleolitico Inferior y Medio. Huelva en su Historia I, 43–56 (1986).

44.
Viehmann, I. Prehistoric Human Footprints in Romania’s Caves. Theor. Appl. Karstol. 3, 229–234 (1987).
Google Scholar 

45.
Harvati, K. The human fossil record from Romania: Early Upper Paleolithic European Mandibles and Neanderthal. (eds Harvati, K. & Roksandic, M.) 51–68 (Springer Netherlands, 2016).

46.
Zazo, C. et al. Pleistocene and Holocene Aeolian facies along the Huelva coast (southern Spain): Climatic and neotectonic implications. Geol. Mijn. 77, 209–224 (1999).
Article  Google Scholar 

47.
Zazo, C. et al. El complejo eólico de El Abalario (Huelva) (eds Sanjaume, E., Gracia, F. J.) 407–425 (Sociedad Española de Geomorfología, Madrid, 2011)

48.
Paerl, H. W. & Yanarell, A. C. Environmental dynamics, community structure and function in a hypersaline microbial mat (eds Seckbach, J. & Oren, A.) 421–442, (Springer Netherlands, 2010).

49.
Porada, H. & Bouougri, E. Wrinkle structures—a critical review (eds Schieber, J. et al.) 135–144 (Elsevier, 2007).

50.
Gerdes, G. What Are Microbial Mats? (eds Seckbach, J. & Oren, A.) 3–25, (Springer Netherlands, 2010).

51.
Eriksson, P. G. et al. Paleoenvironmental Context Of Microbial Mat-Related Structures In Siliciclastic Rocks. (eds Seckbach, J. & Oren, A.) 71–108 (Springer Netherlands, 2010).

52.
Zilhão, J. et al. Last Interglacial Iberian Neandertals as fisher-hunter-gatherers. Science 367, 1443 (2020).
ADS  Article  CAS  Google Scholar 

53.
Hardy, B. L. & Moncel, M.-H. Neanderthal use of fish, mammals, birds, starchy plants and wood 125–250,000 years ago. PLoS ONE 6, e23768 (2011).
ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

54.
Wall-Scheffler, C. M., Wagnild, J. & Wagler, E. Human footprint variation while performing load bearing tasks. PLoS ONE 10, e0118619 (2015).
PubMed  PubMed Central  Article  CAS  Google Scholar 

55.
Romagnoli, F., Martini, F. & Sarti, L. Neanderthal use of Callista chione shells as raw material for retouched tools in South-East Italy: Analysis of Grotta del Cavallo layer l assemblage with a new methodology. J. Archaeol. Method Theory 22, 1007–1037 (2015).
Article  Google Scholar 

56.
Benito, B. M. et al. The ecological niche and distribution of Neanderthals during the Last Interglacial. J. Biogeogr. 44, 51–61 (2017).
Article  Google Scholar 

57.
Villa, P. et al. Neandertals on the beach: Use of marine resources at Grotta dei Moscerini (Latium, Italy). PLoS ONE 15, e0226690 (2020).
CAS  PubMed  PubMed Central  Article  Google Scholar 

58.
Cortés-Sánchez, M. et al. Shellfish collection on the westernmost Mediterranean, Bajondillo cave (~ 160–35 cal kyr BP): A case of behavioral convergence?. Quat. Sci. Rev. 217, 284–196 (2019).
ADS  Article  Google Scholar 

59.
Stringer, C. B. et al. Neandertal exploitation of marine mammals in Gibraltar. PNAS 105, 14319–14324 (2008).
ADS  CAS  PubMed  Article  PubMed Central  Google Scholar  More

1.
Naeem, S., Duffy, J. E. & Zavaleta, E. The functions of biological diversity in an age of extinction. Science 336, 1401–1406 (2012).
ADS  CAS  PubMed  Article  Google Scholar 
2.
Curtis, P. G., Slay, C. M., Harris, N. L., Tyukavina, A. & Hansen, M. C. Classifying drivers of global forest loss. Science 361, 1108–1111 (2018).
ADS  CAS  PubMed  Article  Google Scholar 

3.
Ewers, R. M. & Didham, R. K. Confounding factors in the detection of species responses to habitat fragmentation. Biol. Rev. 81, 117–142 (2006).
PubMed  Article  Google Scholar 

4.
Jones, G., Jacobs, D. S., Kunz, T. H., Willig, M. R. & Racey, P. A. Carpe noctem: the importance of bats as bioindicators. Endanger. Species Res. 8, 93–115 (2009).
Article  Google Scholar 

5.
Rocha, R. et al. Design matters: an evaluation of the impact of small man-made forest clearings on tropical bats using a before-after-control-impact design. For. Ecol. Manag. 401, 8–16 (2017).
Article  Google Scholar 

6.
Wood, J. R. et al. No single driver of biodiversity: divergent responses of multiple taxa across land use types. Ecosphere 8, e01997 (2017).
Article  Google Scholar 

7.
Coutinho Cunto, G. C. & Bernard, E. Neotropical bats as indicators of environmental disturbance: what is the emerging message?. Acta Chiropterologica 14, 143–151 (2012).
Article  Google Scholar 

8.
Medellín, R. A., Equihua, M. & Amin, M. A. Bat diversity and abundance as indicators of disturbance in neotropical rainforest. Conserv. Biol. 14, 1666–1675 (2000).
Article  Google Scholar 

9.
Russo, D., Bosso, L. & Ancillotto, L. Novel perspectives on bat insectivory highlight the value of this ecosystem service in farmland: research frontiers and management implications. Agric. Ecosyst. Environ. 266, 31–38 (2018).
Article  Google Scholar 

10.
Avila-Cabadilla, L. D., Stoner, K. E., Henry, M. & Alvarez Añorve, M. Y. Composition, structure and diversity of phyllostomid bat assemblages in different successional stages of a tropical dry forest. For. Ecol. Manag. 258, 986–996 (2009).
Article  Google Scholar 

11.
Castro-Luna, A. A., Sosa, V. J. & Castillo-Campos, G. Quantifying phyllostomid bats at different taxonomic levels as ecological indicators in a disturbed tropical forest. Acta Chiropterologica 9, 219–228 (2007).
Article  Google Scholar 

12.
García-Morales, R., Badano, E. I. & Moreno, C. E. Response of neotropical bat assemblages to human land use. Conserv. Biol. 27, 1096–1106 (2013).
PubMed  Article  Google Scholar 

13.
Meyer, C. F. J. & Kalko, E. K. V. Bat assemblages on neotropical land-bridge islands: nested subsets and null model analyses of species co-occurrence patterns. Divers. Distrib. 14, 644–654 (2008).
Article  Google Scholar 

14.
Farneda, F. Z. et al. Predicting biodiversity loss in island and countryside ecosystems through the lens of taxonomic and functional biogeography. Ecography 43, 97–106 (2020).
Article  Google Scholar 

15.
Cisneros, L. M., Fagan, M. E. & Willig, M. R. Season-specific and guild-specific effects of anthropogenic landscape modification on metacommunity structure of tropical bats. J. Anim. Ecol. 84, 373–385 (2015).
PubMed  Article  Google Scholar 

16.
Peña-Cuellar, E., Stoner, K. E., Avila-Cabadilla, L. D., Martínez-Ramos, M. & Estrada, A. Phyllostomid bat assemblages in different successional stages of tropical rain forest in Chiapas, Mexico. Biodivers. Conserv. 21, 1381–1397 (2012).
Article  Google Scholar 

17.
Fenton, A. M. B. et al. Phyllostomid bats (Chiroptera: Phyllostomidae) as indicators of habitat disruption in the Neotropics. Biotropica 24, 440–446 (1992).
Article  Google Scholar 

18.
Avila-Cabadilla, L. D. et al. Local and landscape factors determining occurrence of phyllostomid bats in tropical secondary forests. PLoS ONE 7, e35228 (2012).
ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

19.
Falcão, L. A. D., do Espírito-Santo, M. M., Fernandes, G. W. & Paglia, A. P. Effects of habitat structure, plant cover, and successional stage on the bat assemblage of a tropical dry forest at different spatial scales. Diversity 10, 1–11 (2018).
Article  Google Scholar 

20.
Avila-Cabadilla, L. D. et al. Phyllostomid bat occurrence in successional stages of neotropical dry forests. PLoS ONE 9, e84572 (2014).
ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

21.
Falcão, L. A. D., do Espírito-Santo, M. M., Leite, L. O., Garro, R. N. S. L., Avila-Cabadilla, L. D. & Stoner, K. E. Spatiotemporal variation in phyllostomid bat assemblages over a successional gradient in a tropical dry forest in southeastern Brazil. J. Trop. Ecol. 30, 123–132 (2014).
Article  Google Scholar 

22.
Zarazúa-Carbajal, M., Avila-Cabadilla, L. D., Alvarez-Añorve, M. Y., Benítez-Malvido, J. & Stoner, K. E. Importance of riparian habitat for frugivorous bats in a tropical dry forest in western Mexico. J. Trop. Ecol. 33, 74–82 (2017).
Article  Google Scholar 

23.
Meyer, C. F. J., Struebig, M. J. & Willig, M. R. Responses of tropical bats to habitat fragmentation, logging, and deforestation. In Bats in the Anthropocene: conservation of bats in a changing world (eds. Voigt, C. C. & Kingston, T.) 63–103 (Springer International Publishing) doi:https://doi.org/10.1007/978-3-319-25220-9 (2016).

24.
Estrada, A. & Coates-Estrada, R. Bats in continuous forest, forest fragments and in an agricultural mosaic habitat-island at Los Tuxtlas, Mexico. Biol. Conserv. 103, 237–245 (2002).
Article  Google Scholar 

25.
Galindo-González, J. Clasificación de los murciélagos de la región de Los Tuxtlas, Veracruz, respecto a su respuesta a la fragmentación del hábitat. Acta Zoológica Mex. 20, 239–243 (2004).
Google Scholar 

26.
Gorrensen, M. & Willing, M. R. Landscape responses of bats to habitat fragmentation in Atlantic forest of Paraguay. J. Mammal. 85, 688–697 (2004).
Article  Google Scholar 

27.
de Oliveira, H. F. M., de Camargo, N. F., Gager, Y. & Aguiar, L. M. S. The response of bats (Mammalia: Chiroptera) to habitat modification in a neotropical savannah. Trop. Conserv. Sci. 10, 1–14 (2017).
Article  Google Scholar 

28.
de la Peña-Cuéllar, E., Benítez-Malvido, J., Avila-Cabadilla, L. D., Martínez-Ramos, M. & Estrada, A. Structure and diversity of phyllostomid bat assemblages on riparian corridors in a human-dominated tropical landscape. Ecol. Evol. 5, 903–913 (2015).
PubMed  PubMed Central  Article  Google Scholar 

29.
García-Morales, R. et al. Deforestation impacts on bat functional diversity in tropical landscapes. PLoS ONE 11, 1–16 (2016).
Article  CAS  Google Scholar 

30.
Daniel, S., Korine, C. & Pinshow, B. Central-place foraging in nursing, arthropod-gleaning bats. Can. J. Zool. 86, 623–626 (2008).
Article  Google Scholar 

31.
Galindo-González, J. & Sosa, V. J. Frugivorous bats in isolated trees and riparian vegetation associated with human-made pastures in a fragmented tropical landscape. Southwest. Nat. 48, 579–589 (2003).
Article  Google Scholar 

32.
Chazdon, R. L. et al. Rates of change in tree communities of secondary neotropical forests following major disturbances. Philos. Trans. R. Soc. B Biol. Sci. 362, 273–289 (2007).
Article  Google Scholar 

33.
Brito, J., Camacho, M. A., Romero, V. & Vallejo, A. F. Mamíferos del Ecuador. Versión 2019.0. Museo de Zoología, Pontificia Universidad Católica del Ecuador. https://bioweb.bio/faunaweb/mammaliaweb (2019).

34.
Tirira, D. A field guide to the mammals of Ecuador. Asociación Ecuatoriana de Mastozoología and Murciélago Blanco Publishing House (2017).

35.
Jara-Guerrero, A., Maldonado Riofrío, D., Espinosa, C. I. & Duncan, D. H. Beyond the blame game: a restoration pathway reconciles ecologists’ and local leaders’ divergent models of seasonally dry tropical forest degradation. Ecol. Soc. 24, 22 (2019).
Article  Google Scholar 

36.
Cueva Ortiz, J. et al. Influence of anthropogenic factors on the diversity and structure of a dry forest in the central part of the Tumbesian region (Ecuador-Perú). Forests 10, 1–22 (2019).
Article  Google Scholar 

37.
Medina, A., Harvey, C. A., Sánchez Merlo, D., Vílchez, S. & Hernández, B. Bat diversity and movement in an agricultural landscape in Matiguás, Nicaragua. Biotropica 39, 120–128 (2007).
Article  Google Scholar 

38.
Davies, K. F., Margules, C. R. & Lawrence, J. F. Which traits of species predict population declines in experimental forest fragments?. Ecology 81, 1450–1461 (2000).
Article  Google Scholar 

39.
Henle, K., Davies, K. F., Kleyer, M., Margules, C. & Settele, J. Predictors of species sensitivity to fragmentation. Biodivers. Conserv. 13, 207–251 (2004).
Article  Google Scholar 

40.
Medellin, R. A. Chrotopterus auritus. Mamm. Species 343, 1–5 (1989).
Google Scholar 

41.
Aguirre, L. F., Lens, L., Van Damme, R. & Matthysen, E. Consistency and variation in the bat assemblages inhabiting two forest islands within a neotropical savanna in Bolivia. J. Trop. Ecol. 19, 367–374 (2003).
Article  Google Scholar 

42.
Stoner, K. E. Phyllostomid bat community structure and abundance in two contrasting tropical dry forests. Biotropica 37, 591–599 (2005).
Article  Google Scholar 

43.
Gotelli, N. J. & Colwell, R. K. Estimating species richness. In Biological diversity: frontiers in measurement and assessment (eds. Magurran, A. & McGill, B. J.) 39–54 (Oxford University Press, 2011).

44.
Moreno, C. E. & Halffter, G. Assessing the completeness of bat biodiversity inventories using species accumulation curves. J. Appl. Ecol. 37, 149–158 (2000).
Article  Google Scholar 

45.
Colwell, R. K. & Coddington, J. A. Estimating terrestrial biodiversity through extrapolation. Philos. Trans. Biol. Sci. 345, 101–118 (1994).
ADS  CAS  Article  Google Scholar 

46.
Baselga, A. Partitioning the turnover and nestedness components of beta diversity. Glob. Ecol. Biogeogr. 19, 134–143 (2010).
Article  Google Scholar 

47.
Baselga, A. Separating the two components of abundance-based dissimilarity: balanced changes in abundance vs. abundance gradients. Methods Ecol. Evol. 4, 552–557 (2013).
Article  Google Scholar 

48.
Mena, J. L. & Williams de Castro, M. Diversidad y patrones reproductivos de quirópteros en un área urbana de Lima, Perú. Ecol. Apl. 1, 1–8 (2002).
Article  Google Scholar 

49.
Pacheco, V., Cadenillas, R., Salas, E., Tello, C. & Zeballos, H. Diversidad y endemismo de los mamíferos del Perú. Rev. Peru. Biol. 16, 5–32 (2009).
Google Scholar 

50.
Pinto, C. M., Marchán-Rivadeneira, M. R., Tapia, E. E., Carrera, J. P. & Baker, R. J. Distribution, abundance and roosts of the fruit bat Artibeus fraterculus (Chiroptera: Phyllostomidae). Acta Chiropterologica 15, 85–94 (2013).
Article  Google Scholar 

51.
Homyack, J. A. Evaluating habitat quality of vertebrates using conservation physiology tools. Wildl. Res. 37, 332–342 (2010).
Article  Google Scholar 

52.
Carrasco-Rueda, F. & Loiselle, B. A. Do riparian forest strips in modified forest landscapes aid in conserving bat diversity?. Ecol. Evol. 9, 4192–4209 (2019).
PubMed  PubMed Central  Article  Google Scholar 

53.
Lewis, S. E. Roost fidelity of bats: a review. Am. Soc. Mammal. Roost 76, 481–496 (1995).
Google Scholar 

54.
Voss, R. S., Fleck, D. W., Strauss, R. E., Velazco, P. M. & Simmons, N. B. Roosting ecology of Amazonian bats: evidence for guild structure in hyperdiverse mammalian communities. Am. Museum Novit. 3870, 1–43 (2016).
Article  Google Scholar 

55.
Hylander, K. & Ehrle, J. The mechanisms causing extinction debts. Trends Ecol. Evol. 28, 341–346 (2013).
PubMed  Article  Google Scholar 

56.
Willig, M. R. et al. Guild-level responses of bats to habitat conversion in a lowland Amazonian rainforest: species composition and biodiversity. J. Mammal. 100, 223–238 (2019).
PubMed  PubMed Central  Article  Google Scholar 

57.
Meyer, C. F. J. Methodological challenges in monitoring bat population- and assemblage-level changes for anthropogenic impact assessment. Mamm. Biol. 80, 159–169 (2015).
Article  Google Scholar 

58.
Gibb, R., Browning, E., Glover-Kapfer, P. & Jones, K. E. Emerging opportunities and challenges for passive acoustics in ecological assessment and monitoring. Methods Ecol. Evol. 10, 169–185 (2019).
Article  Google Scholar 

59.
Sikes, R. S. & the Animal Care and Use Committee of the American Society of Mammalogists. 2016 Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. J. Mammal. 97, 663–688 (2016).

60.
Espinosa, C. I. et al. Bosques tropicales secos de la región Pacífico Ecuatorial: diversidad, estructura, funcionamiento e implicaciones para la conservación. Ecosistemas 21, 167–179 (2012).
Google Scholar 

61.
García-Cervigón, A. I., Camarero, J. J. & Espinosa, C. I. Intra-annual stem increment patterns and climatic responses in five tree species from an Ecuadorian tropical dry forest. Trees 31, 1057–1067 (2017).
Article  Google Scholar 

62.
Jara-Guerrero, A., De la Cruz, M. & Méndez, M. Seed dispersal spectrum of woody species in South Ecuadorian dry forests: environmental correlates and the effect of considering species abundance. Biotropica 43, 722–730 (2011).
Article  Google Scholar 

63.
Vázquez, M., Larrea, M. & Ojeda, P. Biodiversidad en los bosques secos del suroccidente de la provincia de Loja (EcoCiencia, 2001).
Google Scholar 

64.
Tapia-Armijos, M. F., Homeier, J., Espinosa, C. I., Leuschner, C. & De La Cruz, M. Deforestation and forest fragmentation in south Ecuador since the 1970s-losing a hotspot of biodiversity. PLoS ONE 10, e133701 (2015).
Google Scholar 

65.
Cueva Ortiz, J. & Chalán, L. A. Cobertura vegetal y uso actual del suelo de la provincia de Loja. Informe Técnico (2010).

66.
Kalka, M. & Kalko, E. K. V. Gleaning bats as underestimated predators of herbivorous insects: diet of Micronycteris microtis (Phyllostomidae) in Panama. J. Trop. Ecol. 22, 1–10 (2006).
Article  Google Scholar 

67.
Espinosa, C. I., Valle, D., Armijos, D., Jara-Guerrero, A. & Griffith, D. M. Bat abundance data from Zapotillo, Ecuador 2013–2017. Knowl. Netw. Biocomplexity https://doi.org/10.5063/F1765CQJ (2020).
Article  Google Scholar 

68.
Barwell, L. J., Isaac, N. J. B. & Kunin, W. E. Measuring β-diversity with species abundance data. J. Anim. Ecol. 84, 1112–1122 (2015).
PubMed  PubMed Central  Article  Google Scholar 

69.
Jakob, E. M., Marshall, S. D. & Uetz, G. W. Estimating fitness: a comparison of body condition indices. Oikos 77, 61–67 (1996).
Article  Google Scholar 

70.
Reist, J. D. An empirical evaluation of several univariate methods that adjust for size variation in morphometric data. Can. J. Zool. 63, 1429–1439 (1985).
ADS  Article  Google Scholar 

71.
Oksanen, J. et al. vegan: Community Ecology Package. R package version 2.5-6. https://CRAN.R-project.org/package=vegan (2019).

72.
R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/ (2018). More