Philippa Kaur

1.
Hambright, K. D., Gophen, M. & Serruya, S. Influence of long-term climatic changes on the stratification of a subtropical, warm monomictic lake. Limnol. Oceanogr. 39, 1233–1242 (1994).
ADS  Article  Google Scholar 
2.
Pilla, R. M. et al. Browning-related decreases in water transparency lead to long-term increases in surface water temperature and thermal stratification in two small lakes. J. Geophys. Res. Biogeo. https://doi.org/10.1029/2017JG004321 (2018).
Article  Google Scholar 

3.
Foley, B., Jones, I. D., Maberly, S. C. & Rippey, B. Long-term changes in oxygen depletion in a small temperate lake: Effects of climate change and eutrophication. Freshwater Biol. 57, 278–289 (2012).
CAS  Article  Google Scholar 

4.
Knoll, L. B. et al. Browning-related oxygen depletion in an oligotrophic lake. Inland Waters https://doi.org/10.1080/20442041.2018.1452355 (2018).
Article  Google Scholar 

5.
O’Reilly, C. M., Alin, S. R., Plisnier, P.-D., Cohen, A. S. & McKee, B. A. Climate change decreases aquatic ecosystem productivity of Lake Tanganyika Africa. Nature 424, 766–768 (2003).
ADS  CAS  PubMed  Article  Google Scholar 

6.
Verburg, P., Hecky, R. E. & Kling, H. Ecological consequences of a century of warming in Lake Tanganyika. Science 301, 505–507 (2003).
ADS  CAS  PubMed  Article  Google Scholar 

7.
Saulnier-Talbot, É. et al. Small changes in climate can profoundly alter the dynamics and ecosystem services of tropical crater lakes. PLoS ONE https://doi.org/10.1371/journal.pone.0086561 (2014).
Article  PubMed  PubMed Central  Google Scholar 

8.
Cohen, A. S. et al. Climate warming reduces fish production and benthic habitat in Lake Tanganyika, one of the most biodiverse freshwater ecosystems. P. Natl. Acad. Sci. 113, 9563–9568 (2016).
ADS  CAS  Article  Google Scholar 

9.
Hansen, G. J. A., Read, J. S., Hansen, J. F. & Winslow, L. A. Projected shifts in fish species dominance in Wisconsin lakes under climate change. Glob. Change Biol. 23, 1463–1476 (2017).
ADS  Article  Google Scholar 

10.
De Stasio, B. T., Hill, D. K., Kleinhans, J. M., Nibbelink, N. P. & Magnuson, J. J. Potential effects of global climate change on small north-temperate lakes: Physics, fish, and plankton. Limnol. Oceanogr. 41, 1136–1149 (1996).
ADS  Article  Google Scholar 

11.
Craig, N., Jones, S. E., Weidel, B. C. & Solomon, C. T. Habitat, not resource availability, limits consumer production in lake ecosystems. Limnol. Oceanogr. 60, 2079–2089 (2015).
ADS  Article  Google Scholar 

12.
Brothers, S. et al. A feedback loop links brownification and anoxia in a temperate, shallow lake. Limnol. Oceanogr. 59, 1388–1398 (2014).
ADS  CAS  Article  Google Scholar 

13.
Marotta, H. et al. Greenhouse gas production in low-latitude lake sediments responds strongly to warming. Nat. Clim. Change https://doi.org/10.1038/NCLIMATE2222 (2014).
Article  Google Scholar 

14.
Schneider, P. & Hook, S. J. Space observations of inland water bodies show rapid surface warming since. Geophys. Res. Lett. https://doi.org/10.1029/2010GL045059 (2010).
Article  Google Scholar 

15.
O’Reilly, C. M. et al. Rapid and highly variable warming of lake surface waters around the globe. Geophys. Res. Lett. https://doi.org/10.1002/2015GL066235 (2015).
Article  Google Scholar 

16.
Woolway, R. I. & Merchant, C. J. Worldwide alteration of lake mixing regimes in response to climate change. Nat. Geosci. https://doi.org/10.1038/s41561-019-0322-x (2019).
Article  Google Scholar 

17.
Kraemer, B. M. et al. Morphometry and average temperature affect lake stratification responses to climate change. Geophys. Res. Lett. https://doi.org/10.1002/2015GL064097 (2015).
Article  Google Scholar 

18.
Keller, W., Heneberry, J. & Leduc, J. Linkages between weather, dissolved, organic carbon, and cold-water habitat in a Boreal Shield lake recovering from acidification. Can. J. Fish. Aquat. Sci. 62, 341–347 (2005).
CAS  Article  Google Scholar 

19.
Wagner, A., Volkmann, S. & Dettinger-Klemm, P. M. A. Benthic-pelagic coupling in lake ecosystems: The key role of chironomid pupae as prey of pelagic fish. Ecosphere https://doi.org/10.1890/ES11-00181.1 (2012).
Article  Google Scholar 

20.
Straile, D., Kerimoglu, O. & Peeters, F. Trophic mismatch requires seasonal heterogeneity of warming. Ecology 96, 2794–2805 (2015).
PubMed  Article  PubMed Central  Google Scholar 

21.
Schmid, M. & Köster, O. Excess warming of a Central European lake driven by solar brightening. Water Resour. Res. https://doi.org/10.1002/2016WR018651 (2016).
Article  Google Scholar 

22.
Woolway, R. I., Meinson, P., Nõges, P., Jones, I. D. & Laas, A. Atmospheric stilling leads to prolonged thermal stratification in a large shallow polymictic lake. Clim. Change 141, 759–773 (2017).
Article  Google Scholar 

23.
Read, J. S. & Rose, K. C. Physical responses of small temperate lakes to variation in dissolved organic carbon concentrations. Limnol. Oceanogr. 58, 921–931 (2013).
ADS  CAS  Article  Google Scholar 

24.
Winslow, L. A., Read, J. S., Hansen, G. J. A. & Hanson, P. C. Small lakes show muted climate change signal in deepwater temperatures. Geophys. Res. Lett. https://doi.org/10.1002/2014GL062325 (2015).
Article  Google Scholar 

25.
Morris, D. P. et al. The attenuation of solar UV radiation in lakes and the role of dissolved organic carbon. Limnol. Oceanogr. 40, 1381–1391 (1995).
ADS  CAS  Article  Google Scholar 

26.
Fee, E. J., Hecky, R. E., Kasian, S. E. M. & Cruikshank, D. R. Effects of lake size, water clarity, and climatic variability on mixing depths in Canadian Shield lakes. Limnol. Oceanogr. 41, 912–920 (1996).
ADS  CAS  Article  Google Scholar 

27.
Snucins, E. & Gunn, J. Interannual variation in the thermal structure of clear and colored lakes. Limnol. Oceanogr. 45, 1639–1646 (2000).
ADS  Article  Google Scholar 

28.
Jankowski, T., Livingstone, D. M., Bührer, H., Forster, R. & Niederhauser, P. Consequences of the 2003 European heat wave for lake temperature profiles, thermal stability, and hypolimnetic oxygen depletion: implications for a warmer world. Limnol. Oceanogr. 51, 815–819 (2006).
ADS  Article  Google Scholar 

29.
Downing, J. A. et al. The global abundance and size distribution of lakes, ponds, and impoundments. Limnol. Oceanogr. 51, 2388–2397 (2006).
ADS  Article  Google Scholar 

30.
Maberly, S. C. et al. Global lake thermal regions shift under climate change. Nat. Commun. 11, 1232. https://doi.org/10.1038/s41467-020-15108-z (2020).
ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

31.
IPCC In Climate Change 2013: The Physical Science Basis (eds Stocker, T. F. et al.) (Cambridge University Press, Cambridge, 2013).
Google Scholar 

32.
Pepin, N. et al. Elevation-dependent warming in mountain regions of the world. Nat. Clim. Change https://doi.org/10.1038/NCLIMATE2563 (2015).
Article  Google Scholar 

33.
Rose, K. C., Winslow, L. A., Read, J. S. & Hansen, G. J. A. Climate-induced warming of lakes can be either amplified or suppressed by trends in water clarity. Limnol. Oceanogr. Lett. https://doi.org/10.1002/lol2.10027 (2016).
Article  Google Scholar 

34.
Benson, B. J. et al. Extreme events, trends, and variability in Northern Hemisphere lake-ice phenology (1855–2005). Clim. Change 112, 299–323 (2012).
ADS  Article  Google Scholar 

35.
Sharma, S. et al. Widespread loss of lake ice around the Northern Hemisphere in a warming world. Nat. Clim. Change https://doi.org/10.1038/s41558-018-0393-5 (2019).
Article  Google Scholar 

36.
Woolway, R. I. et al. Global lake responses to climate change. Nat. Rev. Earth. Environ. 1, 388–403 (2020).
ADS  Article  Google Scholar 

37.
Zhang, G. et al. Response of Tibetan Plateau lakes to climate change: Trends, patterns, and mechanisms. Earth Sci. Rev. https://doi.org/10.1016/j.earscirev.2020.103269 (2020).
Article  Google Scholar 

38.
Dokulil, M. T. et al. Twenty years of spatially coherent deepwater warming in lakes across Europe related to the North Atlantic Oscillation. Limnol. Oceanogr. 51, 2787–2793 (2006).
ADS  Article  Google Scholar 

39.
Ficker, H., Luger, M. & Gassner, H. From dimictic to monomictic: Empirical evidence of thermal regime transitions in three deep alpine lakes in Austria induced by climate change. Freshw. Biol. https://doi.org/10.1111/fwb.12946 (2017).
Article  Google Scholar 

40.
Markfort, C. D. et al. Wind sheltering of a lake by a tree canopy or bluff topography. Water Resour. Res. https://doi.org/10.1029/2009WR007759 (2010).
Article  Google Scholar 

41.
Read, J. S. et al. Lake-size dependency of wind shear and convection as controls on gas exchange. Geophys. Res. Lett. https://doi.org/10.1029/2012GL051886 (2012).
Article  Google Scholar 

42.
Beniston, M., Diaz, H. F. & Bradley, R. S. Climatic change at high elevation sites: An overview. Clim. Change 36, 233–251 (1997).
Article  Google Scholar 

43.
Sommaruga-Wögrath, S. et al. Temperature effects on the acidity of remote alpine lakes. Nature 387, 64–67 (1997).
ADS  Article  Google Scholar 

44.
Václavík, T., Lautenback, S., Kuemmerle, T. & Seppelt, R. Mapping global land system archetypes. Glob. Environ. Change https://doi.org/10.1016/j.gloenvcha.2013.09.004 (2013).
Article  Google Scholar 

45.
Bartosiewicz, M. et al. Hot tops, cold bottoms: Synergistic climate warming and shielding effects increase carbon burial in lakes. Limnol. Oceanogr. Lett. https://doi.org/10.1002/lol2.10117 (2019).
Article  Google Scholar 

46.
Williamson, C. E. et al. Ecological consequences of long-term browning in lakes. Sci. Rep. https://doi.org/10.1038/srep18666 (2015).
Article  PubMed  PubMed Central  Google Scholar 

47.
Evans, C. D., Chapman, P. J., Clark, J. M., Monteith, D. T. & Cresser, M. S. Alternative explanations for rising dissolved organic carbon export from organic soils. Glob. Change Biol. 12, 2044–2053 (2006).
ADS  Article  Google Scholar 

48.
Monteith, D. et al. Dissolved organic carbon trends resulting from changes in atmospheric deposition chemistry. Nature https://doi.org/10.1038/nature06316 (2007).
Article  PubMed  Google Scholar 

49.
Couture, S., Houle, D. & Gagnon, C. Increases of dissolved organic carbon in temperate and boreal lakes in Quebec Canada. Environ. Sci. Pollut. Res. 19, 361–371 (2012).
CAS  Article  Google Scholar 

50.
Read, J. S. et al. Derivation of lake mixing and stratification indices from high-resolution lake buoy data. Environ. Model. Softw. 26, 1325–1336 (2011).
Article  Google Scholar 

51.
Gray, E., Mackay, E. B., Elliot, J. A., Folkard, A. M. & Jones, I. D. Wide-spread inconsistency in estimation of lake mixed depth impacts interpretation of limnological processes. Water Res. https://doi.org/10.1016/j.watres.2019.115136 (2020).
Article  PubMed  Google Scholar 

52.
Prokopkin, I. G. & Zadereev, E. S. A model study of the effect of weather forcing on the ecology of a meromictic Siberian Lake. J. Oceanol. Limnol. 36, 2018–2032 (2018).
ADS  CAS  Article  Google Scholar 

53.
Austin, J. A. & Colman, S. M. Lake Superior summer water temperatures are increasing more rapidly than regional air temperatures: A positive ice-albedo feedback. Geophys. Res. Lett. https://doi.org/10.1029/2006GL029021 (2007).
Article  Google Scholar 

54.
Preston, D. L. et al. Climate regulates alpine lake ice cover phenology and aquatic ecosystem structure. Geophys. Res. Lett. https://doi.org/10.1002/2016GL069036 (2016).
Article  Google Scholar 

55.
Sadro, S., Melack, J. M., Sickman, J. O. & Skeen, K. Climate warming response of mountain lakes affected by variations in snow. Limnol. Oceanogr. Lett. https://doi.org/10.1002/lol2.10099 (2018).
Article  Google Scholar 

56.
Zhang, G. et al. Estimating surface temperature changes of lakes in the Tibetan Plateau using MODIS LST data. J. Geophys. Res. Atmos. 119, 8552–8567 (2014).
ADS  Article  Google Scholar 

57.
Taylor, C. A. & Stefan, H. G. Shallow groundwater temperature response to climate change and urbanization. J. Hydrol. 375, 601–612 (2009).
ADS  CAS  Article  Google Scholar 

58.
Zhang, X. Conjunctive surface water and groundwater management under climate change. Front. Environ. Sci. https://doi.org/10.3389/fenvs.2015.00059 (2015).
Article  Google Scholar 

59.
Gaiser, E. E., Deyrup, N. D., Bachmann, R. W., Battoe, L. E. & Swain, H. M. Effects of climate variability on transparency and thermal structure in subtropical, monomictic Lake Annie Florida. Fund. Appl. Limnol. 175, 217–230 (2009).
Article  Google Scholar 

60.
Zhang, J. et al. Long-term patterns of dissolved organic carbon in lakes across eastern Canada: Evidence of a pronounced climate effect. Limnol. Oceanogr. 55, 30–42 (2010).
ADS  CAS  Article  Google Scholar 

61.
Williamson, C. E. et al. Sentinel responses to droughts, wildfires, and floods: effects of UV radiation on lakes and their ecosystem services. Front. Ecol. Environ. 14, 102–109 (2016).
Article  Google Scholar 

62.
Thiery, W. et al. Understanding the performance of the Flake model over two African Great Lakes. Geosci. Model Dev. 7, 317–337 (2014).
ADS  Article  Google Scholar 

63.
Shatwell, T., Thiery, W. & Kirillin, G. Future projections of temperature and mixing regime of European temperate lakes. Hydrol. Earth Syst. Sci. 23, 1533–1551 (2019).
ADS  Article  Google Scholar 

64.
Winslow, L. A., Read, J. S., Hansen, G. J. A., Rose, K. C. & Robertson, D. M. Seasonality of change: summer warming rates do not fully represent effects of climate change on lake temperatures. Limnol. Oceanogr. 62, 2168–2178 (2017).
ADS  Article  Google Scholar 

65.
Fang, X. & Stefan, H. G. Simulations of climate effects on water temperatures, dissolved oxygen, and ice and snow covers in lakes of the contiguous United States under past and future climate scenarios. Limnol. Oceanogr. 54, 2359–2370 (2009).
ADS  CAS  Article  Google Scholar 

66.
Rösner, R., Müller-Navarra, D. C. & Zorita, E. Trend analysis of weekly temperatures and oxygen concentrations during summer stratification in Lake Plußsee: a long-term study. Limnol. Oceanogr. 57, 1479–1491 (2012).
ADS  Article  CAS  Google Scholar 

67.
Rogora, M. et al. Climatic effects on vertical mixing and deep-water oxygen content in the subalpine lakes in Italy. Hydrobiologia 824, 33–50 (2018).
CAS  Article  Google Scholar 

68.
Wilhelm, S. & Adrian, R. Impact of summer warming on the thermal characteristics of a polymictic lake and consequences for oxygen, nutrients and phytoplankton. Freshw. Biol. 53, 226–237 (2008).
CAS  Article  Google Scholar 

69.
North, R. P., North, R. L., Livingstone, D. M., Köster, O. & Kipfer, R. Long-term changes in hypoxia and soluble reactive phosphorus in the hypolimnion of a large temperate lake: consequences of a climate regime shift. Glob. Change Biol. https://doi.org/10.1111/gcb.12371 (2014).
Article  Google Scholar 

70.
Zadereev, E. S., Tolomeev, A. P., Drobotov, A. V. & Kolmakova, A. A. Impact of weather variability on spatial and seasonal dynamics of dissolved and suspended nutrients in water column of meromictic Lake Shira. Contemp. Probl. Ecol. 21, 515–530 (2014).
Google Scholar 

71.
Couture, R.-M., deWit, H. A., Tominaga, K., Kiuru, P. & Markelov, I. Oxygen dynamics in a boreal lake responds to long-term changes in climate, ice phenology, and DOC inputs. J. Geophys. Res. Biogeo. https://doi.org/10.1002/2015JG003065 (2015).
Article  Google Scholar 

72.
Richardson, D. C. et al. Transparency, geomorphology and mixing regime explain variability in trends in lake temperature and stratification across Northeastern North America (1975–2004). Water https://doi.org/10.3390/w9060442 (2017).
Article  Google Scholar 

73.
Kalff, J. Limnology: Inland Water Ecosystems (Prentice Hall, Upper Saddle River, 2002).
Google Scholar 

74.
Wetzel, R. G. Limnology: Lake and River Ecosystems (Academic Press, New York, 2001).
Google Scholar 

75.
Woolway, R. I. et al. Diel surface temperature range scales with lake size. PLoS ONE https://doi.org/10.1371/journal.pone.0152466 (2016).
Article  PubMed  PubMed Central  Google Scholar 

76.
Williamson, C. E., Fischer, J. M., Bollens, S. M., Overholt, E. P. & Breckenridge, J. K. Toward a more comprehensive theory of zooplankton diel vertical migration: Integrating ultraviolet radiation and water transparency into the biotic paradigm. Limnol. Oceanogr. 56, 1603–1623 (2011).
ADS  Article  Google Scholar 

77.
Winslow, L. et al. rLakeAnalyzer: Lake physics tools. R package version 1.11.4.1. https://CRAN.R-project.org/package=rLakeAnalyzer (2019).

78.
Sen, P. K. Estimates of the regression coefficient based on Kendall’s Tau. J. Am. Stat. Assoc. 63, 1379–1389 (1968).
MathSciNet  MATH  Article  Google Scholar 

79.
Hirsch, R. M., Slack, J. R. & Smith, R. A. Techniques of trend analysis for monthly water quality data. Water Resour. Res. 18, 107–121 (1982).
ADS  Article  Google Scholar 

80.
Jassby, A. D. & Cloern, J. E. wq: Some tools for exploring water quality monitoring data. R package version 0.4.8. https://cran.r-project.org/package=wq (2016).

81.
Leach, T. H. et al. Patterns and drivers of deep chlorophyll maxima structure in 100 lakes: the relative importance of light and thermal stratification. Limnol. Oceanogr. 63, 628–646 (2018).
ADS  CAS  Article  Google Scholar 

82.
Breiman, L. Random forests. Mach. Learn. 45, 5–32 (2001).
MATH  Article  Google Scholar 

83.
James, G., Witten, D., Hastie, T. & Tibshirani, R. Tree-based methods. In An Introduction to Statistical Learning: With Applications in R (Springer, Berlin, 2015).
Google Scholar 

84.
Genuer, R., Poggi, J.-M. & Tuleau-Malot, C. Variable selection using random forests. Pattern Recogn. Lett. 31, 2225–2236 (2010).
Article  Google Scholar 

85.
Dormann, C. F. et al. Collinearity: A review of methods to deal with it and a simulation study evaluating their performance. Ecography 36, 027–046 (2013).
Article  Google Scholar 

86.
Auret, L. & Alrich, C. Interpretation of nonlinear relationships between process variables by use of random forests. Miner. Eng. 35, 27–42 (2012).
CAS  Article  Google Scholar 

87.
Liaw, A. & Wiener, M. Classification and regression by randomForest. R News 2, 18–22 (2002).
Google Scholar 

88.
R Core Team. R: a language and environment for statistical computing, R Foundation for Statistical Computing. https://www.R-project.org/ (2019).

89.
Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, Berlin, 2016).
Google Scholar  More

1.
Prasad, A. M. et al. Modeling the invasive emerald ash borer risk of spread using a spatially explicit cellular model. Landsc. Ecol. 25(3), 353–369 (2010).
Article  Google Scholar 
2.
Huang, D., Zhang, R., Kim, K. C. & Suarez, A. V. Spatial pattern and determinants of the first detection locations of invasive alien species in mainland China. PLoS ONE 7(2), e31734 (2012).
ADS  CAS  Article  Google Scholar 

3.
Roy, H. E. et al. Invasive alien predator causes rapid declines of native European ladybirds. Divers. Distrib. 18(7), 717–725 (2012).
Article  Google Scholar 

4.
Cini, A. et al. Tracking the invasion of the alien fruit pest Drosophila suzukii in Europe. J. Pest Sci. 87(4), 559–566 (2014).
Article  Google Scholar 

5.
Filipe, A. F., Quaglietta, L., Ferreira, M., Magalhães, M. F. & Beja, P. Geostatistical distribution modelling of two invasive crayfish across dendritic stream networks. Biol. Invas. 19(10), 2899–2912 (2017).
Article  Google Scholar 

6.
Hahn, N. G., Rodriguez-Saona, C. & Hamilton, G. C. Characterizing the spatial distribution of brown marmorated stink bug, Halyomorpha halys Stål (Hemiptera: Pentatomidae), populations in peach orchards. PLoS ONE 12(3), e0170889 (2017).
Article  Google Scholar 

7.
Carrière, Y. et al. Effects of local and landscape factors on population dynamics of a cotton pest. PLoS ONE 7(6), e39862 (2012).
ADS  Article  Google Scholar 

8.
Wang, X. G., Kaçar, G., Biondi, A. & Daane, K. M. Foraging efficiency and outcomes of interactions of two pupal parasitoids attacking the invasive spotted wing drosophila. Biol. Control 96, 64–71 (2016).
Article  Google Scholar 

9.
Dara, S. K., Barringer, L. & Arthurs, S. P. Lycorma delicatula (Hemiptera: Fulgoridae): a new invasive pest in the United States. J. Integr. Pest Manage. 6, 1–20 (2015).
Article  Google Scholar 

10.
Kim, H. et al. Molecular comparison of Lycorma delicatula (Hemiptera: Fulgoridae) isolates in Korea, China, and Japan. J. Asia-Pac. Entomol. 16(4), 503–506 (2013).
CAS  Article  Google Scholar 

11.
Han, J. M. et al. Lycorma delicatula (Hemiptera: Auchenorrhyncha: Fulgoridae: Aphaeninae) finally, but suddenly arrived in Korea. Entomol. Res. 38(4), 281–286 (2008).
Article  Google Scholar 

12.
Wakie, T. T., Neven, L. G., Yee, W. L. & Lu, Z. The establishment risk of Lycorma delicatula (Hemiptera: Fulgoridae) in the United States and globally. J. Econ. Entomol. https://doi.org/10.1093/jee/toz259 (2019).
Article  Google Scholar 

13.
Jung, J. M., Jung, S., Byeon, D. & Lee, W. H. Model-based prediction of potential distribution of the invasive insect pest, spotted lanternfly Lycorma delicatula (Hemiptera: Fulgoridae), by using CLIMEX. J. Asia-Pac. Biodivers. 10, 532–538 (2017).
Article  Google Scholar 

14.
Harper, J. K., Stone, W., Kelsey, T. W. & Kime, L. F. Potential economic impact of the spotted lanternfly on agriculture and forestry in Pennsylvania. Control Rural Pennsylvania Rep. 1, 1–84 (2019).
Google Scholar 

15.
Leach, H. & Leach, A. Seasonal phenology and activity of spotted lanternfly (Lycorma delicatula) in eastern US vineyards. J. Pest Sci. https://doi.org/10.1007/s10340-020-01233-7 (2020).
Article  Google Scholar 

16.
Barringer, L. E. & Smyers, E. Predation of the spotted lanternfly, Lycorma delicatula (White) (Hemiptera: Fulgoridae) by two native Hemiptera. Entomol. News 126, 71–73 (2016).
Article  Google Scholar 

17.
Cooperband, M. F., Mack, R. & Spichiger, S. E. Chipping to destroy egg masses of the spotted lanternfly, Lycorma delicatula (Hemiptera: Fulgoridae). J. Insect Sci. 18(3), 7–10 (2018).
Article  Google Scholar 

18.
Leach, H., Biddinger, D. J., Krawczyk, G., Smyer, S. E. & Urban, J. M. Evaluation of insecticides for control of the spotted lanternfly, Lycorma delicatula, (Hemiptera: Fulgoridae), a new pest of fruit in the Northeastern US. Crop Prot. https://doi.org/10.1016/j.cropro.2019.05.027 (2019).
Article  Google Scholar 

19.
Clifton, E. H., Castrillo, L. A., Gryganskyi, A. & Hajek, A. E. A pair of native fungal pathogens drives decline of a new invasive herbivore. Proc. Natl. Acad. Sci. 116(19), 9178–9180 (2019).
CAS  Article  Google Scholar 

20.
Urban, J. M. Perspective: shedding light on spotted lanternfly impacts in the USA. Pest Manage. Sci. https://doi.org/10.1002/ps.5619 (2020).
Article  Google Scholar 

21.
Wolfin, M. S. et al. Flight dispersal capabilities of female spotted lanternflies (Lycorma delicatula) related to size and mating status. J. Insect Behav. 32(3), 188–200 (2019).
Article  Google Scholar 

22.
Clifton, E. H. et al. Applications of Beauveria bassiana (Hypocreales: Cordycipitaceae) to control populations of spotted lanternfly (Hemiptera: Fulgoridae), in semi-natural landscapes and on grapevines. Environ. Entomol. https://doi.org/10.1093/ee/nvaa064 (2020).
Article  PubMed  Google Scholar 

23.
Francese, J. A. et al. Developing traps for the spotted lanternfly, Lycorma delicatula (Hemiptera: Fulgoridae). Environ. Entomol. 49(2), 269–276 (2020).
Article  Google Scholar 

24.
Nguyen, H. D. D. & Nansen, C. Edge-biased distributions of insects. A review. Agron. Sustain. Dev. 38, 11 (2018).
Article  Google Scholar 

25.
Ries, L. & Sisk, T. D. A predictive model of edge effects. Ecology https://doi.org/10.1890/03-8021 (2004).
Article  Google Scholar 

26.
Leskey, T. C., Short, B. D. & Ludwick, D. Comparison and refinement of integrated pest management tactics for Halyomorpha halys (Hemiptera: Pentatomidae) management in apple orchards. J. Econ. Entomol. https://doi.org/10.1093/jee/toaa067 (2020).
Article  PubMed  Google Scholar 

27.
Mason, K. S., Roubos, C. R., Teixeira, L. A. & Isaacs, R. Spatially targeted applications of reduced-risk insecticides for economical control of grape berry moth, Paralobesia viteana (Lepidoptera: Tortricidae). J. Econ. Entomol. 109(5), 2168–2174 (2016).
CAS  Article  Google Scholar 

28.
Goffinet, M.C. Anatomy of grapevine winter injury and recovery. Dept. Hort. Services Res. Paper, Cornell Univ. (2004). Accessed April 20, 2020 from https://www.eaglegrapegrowers.org/uploads/1/1/8/4/118472897/anatomy_of_winter_injury_hi_res.pdf.

29.
Halldorson, M. M. & Keller, M. Grapevine leafroll disease alters leaf physiology but has little effect on plant cold hardiness. Planta 248(5), 1201–1211 (2018).
CAS  Article  Google Scholar 

30.
Süle, S. & Burr, T. J. The effect of resistance of rootstocks to crown gall (Agrobacterium spp.) on the susceptibility of scions in grape vine cultivars. Plant Pathol. 47, 84–88 (1998).
Article  Google Scholar 

31.
Bates, D., Maechler, M., Bolker, B., Walker, S., Christensen, R.H.B., Singmann, H., Dai, B., Scheipl, F., Grothendieck, G. & Green, P. R Package ‘lme4’. 1.17 (2018).

32.
Bartoń, K. MuMIn: Multi-model Inference. R Package version 1.40.4 (2018).

33.
Korner-Nievergelt, F. et al. Bayesian Data Analysis in Ecology Using Linear Models with R, BUGS and Stan (Elsevier, Hoboken, 2015).
Google Scholar 

34.
Anselin, L. Local indicators of spatial association—LISA. Geogr. Anal. 27(2), 93–115 (1995).
Article  Google Scholar 

35.
Mitchell, A. The ESRI Guide to GIS Analysis (ESRI Press, Redlands, 2005).
Google Scholar 

36.
Krivoruchko, K. Spatial Statistical Data Analysis for GIS Users 928 (ESRI Press, Redland, 2011).
Google Scholar  More

1.
Worm, B. et al. Rebuilding global fisheries. Science 325, 578–585 (2009).
ADS  CAS  PubMed  Article  Google Scholar 
2.
Costello, C. et al. Global fishery prospects under contrasting management regimes. Proc. Natl Acad. Sci. USA 113, 5125–5129 (2016).
ADS  CAS  PubMed  Article  Google Scholar 

3.
Allan, J. D. et al. Overfishing of inland waters. Bioscience 55, 1041–1051 (2005).
Article  Google Scholar 

4.
Lester, S. E. et al. Biological effects within no-take marine reserves: a global synthesis. Mar. Ecol. Prog. Ser. 384, 33–46 (2009).
ADS  Article  Google Scholar 

5.
Halpern, B. S., Lester, S. E. & McLeod, K. L. Placing marine protected areas onto the ecosystem-based management seascape. Proc. Natl Acad. Sci. USA 107, 18312–18317 (2010).
ADS  CAS  PubMed  Article  Google Scholar 

6.
Carr, M. H. et al. Marine protected areas exemplify the evolution of science and policy. Oceanography (Wash. D.C.) 32, 94–103 (2019).
Article  Google Scholar 

7.
Gaines, S. D., White, C., Carr, M. H. & Palumbi, S. R. Designing marine reserve networks for both conservation and fisheries management. Proc. Natl Acad. Sci. USA 107, 18286–18293 (2010).
ADS  CAS  PubMed  Article  Google Scholar 

8.
Edgar, G. J. et al. Global conservation outcomes depend on marine protected areas with five key features. Nature 506, 216–220 (2014).
ADS  CAS  PubMed  Article  Google Scholar 

9.
Abell, R., Lehner, B., Thieme, M. & Linke, S. Looking beyond the fenceline: assessing protection gaps for the world’s rivers. Conserv. Lett. 10, 384–394 (2017).
Article  Google Scholar 

10.
Grill, G. et al. Mapping the world’s free-flowing rivers. Nature 569, 215–221 (2019).
ADS  CAS  PubMed  Article  Google Scholar 

11.
Vörösmarty, C. J. et al. Global threats to human water security and river biodiversity. Nature 467, 555–561 (2010).
ADS  PubMed  Article  CAS  Google Scholar 

12.
McIntyre, P. B., Reidy Liermann, C. A. & Revenga, C. Linking freshwater fishery management to global food security and biodiversity conservation. Proc. Natl Acad. Sci. USA 113, 12880–12885 (2016).
CAS  PubMed  Article  Google Scholar 

13.
Fluet-Chouinard, E., Funge-Smith, S. & McIntyre, P. B. Global hidden harvest of freshwater fish revealed by household surveys. Proc. Natl Acad. Sci. USA 115, 7623–7628 (2018).
CAS  PubMed  Article  Google Scholar 

14.
Golden, C. D. et al. Nutrition: Fall in fish catch threatens human health. Nature 534, 317–320 (2016).
ADS  PubMed  Article  Google Scholar 

15.
Botsford, L. W., Micheli, F. & Hastings, A. Principles for the design of marine reserves. Ecol. Appl. 13, 25–31 (2003).
Article  Google Scholar 

16.
Gell, F. R. & Roberts, C. M. Benefits beyond boundaries: the fishery effects of marine reserves. Trends Ecol. Evol. 18, 448–455 (2003).
Article  Google Scholar 

17.
Hastings, A. & Botsford, L. W. Comparing designs of marine reserves for fisheries and for biodiversity. Ecol. Appl. 13, 65–70 (2003).
Article  Google Scholar 

18.
Pendleton, L. H. et al. Debating the effectiveness of marine protected areas. ICES J. Mar. Sci. 75, 1156–1159 (2018).
Article  Google Scholar 

19.
Chessman, B. C. Do protected areas benefit freshwater species? A broad-scale assessment for fish in Australia’s Murray–Darling Basin. J. Appl. Ecol. 50, 969–976 (2013).
Article  Google Scholar 

20.
Lawrence, D. J. et al. National parks as protected areas for U.S. freshwater fish diversity. Conserv. Lett. 4, 364–371 (2011).
Article  Google Scholar 

21.
Abell, R. et al. Concordance of freshwater and terrestrial biodiversity. Conserv. Lett. 4, 127–136 (2011).
Article  Google Scholar 

22.
Hilborn, R. Policy: Marine biodiversity needs more than protection. Nature 535, 224–226 (2016).
ADS  CAS  PubMed  Article  Google Scholar 

23.
Halpern, B. S. et al. Achieving the triple bottom line in the face of inherent trade-offs among social equity, economic return, and conservation. Proc. Natl Acad. Sci. USA 110, 6229–6234 (2013).
ADS  CAS  PubMed  Article  Google Scholar 

24.
Gill, D. A. et al. Capacity shortfalls hinder the performance of marine protected areas globally. Nature 543, 665–669 (2017).
ADS  CAS  PubMed  Article  Google Scholar 

25.
Baird, I. G., Flaherty, M. S. & Baird, I. G. Mekong River fish conservation zones in southern Laos: assessing effectiveness using local ecological knowledge. Environ. Manage. 36, 439–454 (2005).
PubMed  Article  Google Scholar 

26.
Loury, E. K. et al. Salty stories, fresh spaces: lessons for aquatic protected areas from marine and freshwater experiences. Aquat. Conserv. 28, 485–500 (2018).
Article  Google Scholar 

27.
McCann, K. S. et al. Food webs and the sustainability of indiscriminate fisheries. Can. J. Fish. Aquat. Sci. 73, 656–665 (2016).
CAS  Article  Google Scholar 

28.
Gutiérrez, N. L., Hilborn, R. & Defeo, O. Leadership, social capital and incentives promote successful fisheries. Nature 470, 386–389 (2011).
ADS  PubMed  Article  CAS  Google Scholar 

29.
Kramer, D. L. & Chapman, M. R. Implications of fish home range size and relocation for marine reserve function. Environ. Biol. Fishes 55, 65–79 (1999).
Article  Google Scholar 

30.
Morrison, S. A. A framework for conservation in a human-dominated world. Conserv. Biol. 29, 960–964 (2015).
PubMed  Article  Google Scholar 

31.
Campos-Silva, J. V. & Peres, C. A. Community-based management induces rapid recovery of a high-value tropical freshwater fishery. Sci. Rep. 6, 34745 (2016).
ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

32.
Castello, L., Viana, J. P., Watkins, G., Pinedo-Vasquez, M. & Luzadis, V. A. Lessons from integrating fishers of arapaima in small-scale fisheries management at the Mamirauá Reserve, Amazon. Environ. Manage. 43, 197–209 (2009).
ADS  PubMed  Article  Google Scholar 

33.
Pinho, P. F., Orlove, B. & Lubell, M. Overcoming barriers to collective action in community-based fisheries management in the Amazon. Hum. Organ. 71, 99–109 (2012).
Article  Google Scholar 

34.
Thompson, P. M., Sultana, P. & Islam, N. Lessons from community based management of floodplain fisheries in Bangladesh. J. Environ. Manage. 69, 307–321 (2003).
PubMed  Article  Google Scholar 

35.
Alexander, S. M., Epstein, G., Bodin, Ö., Armitage, D. & Campbell, D. Participation in planning and social networks increase social monitoring in community-based conservation. Conserv. Lett. 11, e12562 (2018).
Article  Google Scholar 

36.
Ostrom, E. A general framework for analyzing sustainability of social-ecological systems. Science 325, 419–422 (2009).
ADS  MathSciNet  CAS  PubMed  MATH  Article  Google Scholar 

37.
Halpern, B. S., Lester, S. E. & Kellner, J. B. Spillover from marine reserves and the replenishment of fished stocks. Environ. Conserv. 36, 268–276 (2009).
Article  Google Scholar 

38.
Campbell Grant, E. H., Lowe, W. H. & Fagan, W. F. Living in the branches: population dynamics and ecological processes in dendritic networks. Ecol. Lett. 10, 165–175 (2007).
PubMed  Article  Google Scholar 

39.
Palumbi, S. R. Population genetics, demographic connectivity, and the design of marine reserves. Ecol. Appl. 13, 146–158 (2003).
Article  Google Scholar 

40.
Tilman, D., May, R. M., Lehman, C. L. & Nowak, M. A. Habitat destruction and the extinction debt. Nature 371, 65–66 (1994).
ADS  Article  Google Scholar 

41.
McIntyre, P. B. et al. in Conservation of Freshwater Fishes (eds Closs, G. P. et al.) 324–360 (Cambridge Univ. Press, 2015).

42.
Dudgeon, D. et al. Freshwater biodiversity: importance, threats, status and conservation challenges. Biol. Rev. Camb. Philos. Soc. 81, 163–182 (2006).
PubMed  Article  Google Scholar 

43.
Roberts, C. M. et al. Marine reserves can mitigate and promote adaptation to climate change. Proc. Natl Acad. Sci. USA 114, 6167–6175 (2017).
ADS  CAS  PubMed  Article  Google Scholar 

44.
Koning, A. A., Moore, J., Suttidate, N., Hannigan, R. & McIntyre, P. B. Aquatic ecosystem impacts of land sharing versus sparing: nutrient loading to Southeast Asian rivers. Ecosystems (N. Y.) 20, 393–405 (2017).
CAS  Article  Google Scholar 

45.
Froese, R. & Pauly, D. (eds) FishBase http://www.fishbase.org (2019).

46.
Lamberti, G. A. & Hauer, F. R. Methods in Stream Ecology (Academic, 2017).

47.
Jari Oksanen, F. et al. vegan: Community Ecology Package. R package version 2.5-6 https://CRAN.R-project.org/package=vegan (2019).

48.
R Core Team. R: A Language and Environment for Statistical Computing https://www.R-project.org/ (R Foundation for Statistical Computing, 2019).

49.
Google Earth (November, 2015). Mae Ngao, Thailand. https://www.google.co.uk/earth/ (2020).

50.
Environmental Systems Research Institute (ESRI). ArcGIS Release 10.3 (2015).

51.
Yamazaki, D. et al. A high-accuracy map of global terrain elevations. Geophys. Res. Lett. 44, 5844–5853 (2017).
ADS  Article  Google Scholar 

52.
Robin, X. et al. pROC: an open-source package for R and S+ to analyze and compare ROC curves. BMC Bioinformatics 12, 77 (2011).
PubMed  PubMed Central  Article  Google Scholar 

53.
Jordán, F., Liu, W. C. & Andrew, J. D. Topological keystone species: measures of positional importance in food webs. Oikos 112, 535–546 (2006).
Article  Google Scholar 

54.
Bates, D., Maechler, M. & Ben Bolker, S. W. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).
Article  Google Scholar 

55.
Claudet, J. et al. Marine reserves: size and age do matter. Ecol. Lett. 11, 481–489 (2008).
PubMed  Article  Google Scholar 

56.
Claudet, J. et al. Marine reserves: fish life history and ecological traits matter. Ecol. Appl. 20, 830–839 (2010).
CAS  PubMed  Article  Google Scholar 

57.
Johnson, J. B. & Omland, K. S. Model selection in ecology and evolution. Trends Ecol. Evol. 19, 101–108 (2004).
PubMed  Article  Google Scholar 

58.
Barton, K. MuMIn: Multi-Model Inference. R package version 1.43.6 https://CRAN.R-project.org/package=MuMIn (2019). More

1.
Vilaseca, M., Gutiérrez, M. C., López-Grimau, V., López-Mesas, M. & Crespi, M. Biological treatment of a textile effluent after electrochemical oxidation of reactive dyes. Water Environ. Res. 82, 176–182 (2010).
CAS  PubMed  Article  PubMed Central  Google Scholar 
2.
Mahmood, Q., Mahnoor, A., Shahida, S., Tahir, M. & Ali, S. Cadmium contamination in water and soil. In Cadmium Toxic (eds Hasanuzzaman, M. et al.) 141–161 (Elsevier, Amsterdam, Toler. Plants, 2018).
Google Scholar 

3.
Wasi, S., Tabrez, S. & Ahmad, M. Toxicological effects of major environmental pollutants: an overview. Environ. Monit. Assess. 185, 2585–2593 (2013).
PubMed  Article  Google Scholar 

4.
Malik, A. Environmental challenge vis a vis opportunity: the case of water hyacinth. Environ. Int. 33, 122–138 (2007).
CAS  PubMed  Article  Google Scholar 

5.
Asere, T. G., Stevens, C. V. & Du Laing, G. Use of (modified) natural adsorbents for arsenic remediation: a review. Sci. Total Environ. 676, 706–720 (2019).
ADS  CAS  PubMed  Article  Google Scholar 

6.
Shakoor, M. B. et al. Remediation of arsenic contaminated water using agricultural wastes as biosorbents. Crit. Rev. Environ. Sci. Technol. 46, 467–499 (2016).
CAS  Article  Google Scholar 

7.
Bilal, M., et al. Waste biomass adsorbents for copper removal from industrial wastewater—a review. J. Hazard. Mater. 263Pt 2, 322–333 (2013).

8.
Lesmana, S. O., Febriana, N., Soetaredjo, F. E., Sunarso, J. & Ismadji, S. Studies on potential applications of biomass for the separation of heavy metals from water and wastewater. Biochem. Eng. J. 44, 19–41 (2009).
CAS  Article  Google Scholar 

9.
Ofomaja, A. E. & Ho, Y. S. Effect of pH on cadmium biosorption by coconut copra meal. J. Hazard. Mater. 139, 356–362 (2007).
CAS  PubMed  Article  Google Scholar 

10.
Saied, S., Gebauer, J., Hammer, K. & Buerkert, A. Ziziphus spina-christi (L.) willd: a multipurpose fruit tree. Genet. Resour. Crop Evol. 55, 929–937 (2008).
Article  Google Scholar 

11.
Omri, A. & Benzina, M. Characterization of activated carbon prepared from a new raw lignocellulosic material: Ziziphus Spina-Christi seeds. J. Soc. Chim. Tunisie 14, 175–183 (2012).
Google Scholar 

12.
Nazif, N.M. Phytoconstituents of Zizyphus spina-christi L. fruits and their antimicrobial activity. Food Chem. 76, 77–81 (2002).
CAS  Article  Google Scholar 

13.
Amoo, I. A. & Atasie, V. N. Nutritional and functional properties of Tamarindus Indica Pulp and Zizyphus spina-christi fruit and seed. J. Food Agric. Environ. 10, 16–19 (2012).
CAS  Google Scholar 

14.
Osman, M. A. & Ahmed, M. A. Chemical and proximate composition of (Zizyphus spina-christi) Nabag Fruit. Nutr. Food Sci. 39, 70–75 (2009).
Article  Google Scholar 

15.
Ngah, W. S. W. & Hanafiah, M. A. K. M. Removal of heavy metal ions from wastewater by chemically modified plant wastes as adsorbents: a review. Bioresour. Technol. 99, 3935–3948 (2008).
Article  CAS  Google Scholar 

16.
Gautam, R.K., Chattopadhyaya, M.C. & Sharma, S.K. Biosorption of heavy metals: recent trends and challenges Ravindra. In Wastewater Reuse and Management; (Sharma, S.K., Sanghi, R., Eds).; Springer: Berlin, 305–322 (2013).

17.
Park, D., Yun, Y.-S. & Park, J. M. The past, present, and future trends of biosorption. Biotechnol. Bioprocess Eng. 15, 86–102 (2010).
CAS  Article  Google Scholar 

18.
Won, S. W., Kotte, P., Wei, W., Lim, A. & Yun, Y.-S. Biosorbents for recovery of precious metals. Bioresour. Technol. 160, 203–212 (2014).
CAS  PubMed  Article  Google Scholar 

19.
Patel, S. Potential of fruit and vegetable wastes as novel biosorbents: summarizing the recent studies. Rev. Environ. Sci. Bio/Technol. 11, 365–380 (2012).
CAS  Article  Google Scholar 

20.
Volesky, B. Biosorption and me. Water Res. 41, 4017–4029 (2007).
CAS  PubMed  Article  Google Scholar 

21.
Vijayaraghavan, K. & Yun, Y. S. Bacterial biosorbents and biosorption. Biotechnol. Adv. 26, 266–291 (2008).
CAS  PubMed  Article  Google Scholar 

22.
Acar, F. N. & Eren, Z. Removal of Cu(II) ions by activated poplar sawdust (Samsun Clone) from aqueous solutions. J. Hazard. Mater. 137, 909–914 (2006).
CAS  PubMed  Article  Google Scholar 

23.
Reddy, B. R., Mirghaffari, N. & Gaballah, I. Removal and recycling of copper from aqueous solutions using treated Indian barks. Resour. Conserv. Recycl. 21, 227–245 (1997).
Article  Google Scholar 

24.
Su, P., Zhang, J., Tang, J. & Zhang, C. Preparation of nitric acid modified powder activated carbon to remove trace amount of Ni(II) in aqueous solution. Water Sci. Technol. 80, 86–97 (2019).
CAS  PubMed  Article  Google Scholar 

25.
Sciban, M., Klasnja, M. & Skrbic, B. Modified softwood sawdust as adsorbent of heavy metal ions from water. J. Hazard. Mater. 136, 266–271 (2006).
CAS  PubMed  Article  Google Scholar 

26.
Taty-Costodes, V. C., Fauduet, H., Porte, C. & Delacroix, A. Removal of Cd(II) and Pb(II) ions, from aqueous solutions, by adsorption onto sawdust of Pinus sylvestris. J. Hazard. Mater. 105, 121–142 (2003).
CAS  PubMed  Article  Google Scholar 

27.
Gupta, V. K., Jain, C. K., Ali, I., Sharma, M. & Saini, V. K. Removal of cadmium and nickel from wastewater using bagasse fly ash—a sugar industry waste. Water Res. 37, 4038–4044 (2003).
CAS  PubMed  Article  Google Scholar 

28.
Polatoğlu, I. & Karataş, D. Modeling of molecular interaction between catechol and tyrosinase by DFT. J. Mol. Struct. 1202, 127192 (2020).
Article  CAS  Google Scholar 

29.
Omar, A., Ezzat, H., Elhaes, H. & Ibrahim, M. A. Molecular modeling analyses for modified biopolymers. Biointerface Res. Appl. Chem. 11(1), 7847–7859 (2021).
Google Scholar 

30.
Badry, R. et al. Spectroscopic and thermal analyses for the effect of acetic acid on the plasticized sodium carboxymethyl cellulose. J. Mol. Struct. 1224, 129013 (2021).
CAS  Article  Google Scholar 

31.
Menazea, A. A. et al. Chitosan/graphene oxide composite as an effective removal of Ni, Cu, As, Cd and Pb from wastewater. Comput. Theor. Chem. 1189, 112980 (2020).
CAS  Article  Google Scholar 

32.
Al-Bagawi, A. H., Bayoumy, A. M. & Ibrahim, M. A. Molecular modeling analyses for graphene functionalized with Fe3O4 and NiO. Heliyon 6(7), e04456 (2020).
PubMed  PubMed Central  Article  Google Scholar 

33.
Assirey, E. A., Sirry, S. M., Burkani, H. A. & Ibrahim, M. Biosorption of zinc(II) and cadmium(II) using Ziziphus spina stones. J. Comput. Theor. Nanosci. 15, 3102–3108 (2018).
CAS  Article  Google Scholar 

34.
Rice, E. W., Baird, R. B., Eaton, A. D. & Clesceri, L. S. Standard Methods for the Examination of Water and Wastewater 23rd edn. (American Public Health Association (APHA), Washington, DC, 2017).
Google Scholar 

35.
Zhang, B. et al. Biosorption characteristics of Bacillus gibsonii S-2 waste biomass for removal of lead (II) from aqueous solution. Environ. Sci. Pollut. Res. Int. 20, 1367–1373 (2013).
CAS  PubMed  Article  PubMed Central  Google Scholar 

36.
Langmuir, I. The adsorption of gases on plane surfaces of glass, mica and platinum. J. Am. Chem. Soc. 40, 1361–1403 (1918).
CAS  Article  Google Scholar 

37.
Frisch, M. et al. Gaussian 09, revision C.01 (Gaussian, Inc., Wallingford, 2009).

38.
Becke, A. D. Density-functional thermochemistry—III: the role of exact exchange. Chem. Phys. 98, 5648 (1993).
ADS  CAS  Google Scholar 

39.
Lee, C., Yang, W. & Parr, R. G. Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density. Phys. Rev. B 37, 785 (1988).
ADS  CAS  Article  Google Scholar 

40.
Miehlich, B., Savin, A., Stoll, H. & Preuss, H. Results obtained with the correlation energy density functionals of Becke and Lee Yang and Parr. Chem. Phys. Lett. 157, 200–206 (1989).
ADS  CAS  Article  Google Scholar 

41.
Jin, Y., Zhang, Y., Lü, Q. & Cheng, X. Biosorption of methylene blue by chemically modified cellulose waste. J. Wuhan Univ. Technol. Sci. Ed. 29, 817–823 (2014).
CAS  Article  Google Scholar 

42.
Calero, M., Pérez, A., Blázquez, G., Ronda, A. & Martín-Lara, M. A. Characterization of chemically modified biosorbents from olive tree pruning for the biosorption of lead. Ecol. Eng. 58, 344–354 (2013).
Article  Google Scholar 

43.
Abdolali, A. et al. Characterization of a multi-metal binding biosorbent: chemical modification and desorption studies. Bioresour. Technol. 193, 477–487 (2015).
CAS  PubMed  Article  Google Scholar 

44.
Brigida, A. I. S., Calado, V. M. A., Goncalves, L. R. B. & Coelho, M. A. Z. Effect of chemical treatments on properties of green coconut fiber. Carbohydr. Polym. 79, 832–838 (2010).
CAS  Article  Google Scholar 

45.
Herrera-Franco, P. J. & Valadez-Gonzalez, A. A. Study of the mechanical properties of short natural-fiber reinforced composites. Compos. Part B Eng. 36, 597–608 (2005).
Article  CAS  Google Scholar 

46.
Mao, J., Won, S. W., Choi, S. B., Lee, M. W. & Yun, Y. S. Surface modification of the Corynebacterium Glutamicum biomass to increase carboxyl binding site for basic dye molecules. Biochem. Eng. J. 46, 1–6 (2009).
Article  CAS  Google Scholar 

47.
Ramana, D. K. V., Reddy, K. D. H., Kumar, B. N., Harinath, Y. & Seshaiah, K. Removal of nickel from aqueous solutions by citric acid modified Ceiba Pentandra Hulls: equilibrium and kinetic studies. Can. J. Chem. Eng. 90, 111–119 (2012).
CAS  Article  Google Scholar 

48.
Martín-Lara, M. A., Pagnanelli, F., Mainelli, S., Calero, M. & Toro, L. Chemical treatment of olive Pomace: effect on acid-basic properties and metal biosorption capacity. J. Hazard. Mater. 2012(156), 448–457 (2012).
Google Scholar 

49.
Shadreck, M., Chigondo, F., Shumba, M., Nyamunda, B. C. & Edith, S. Removal of chromium (VI) from aqueous solution using chemically modified orange (Citrus Cinensis) peel. IOSR J. Appl. Chem. 6, 66–75 (2013).
Article  Google Scholar 

50.
Olu-owolabi, B. I., Oputu, O. U., Adebowale, K. O., Ogonsolu, O. & Olujimi, O. O. Biosorption of Cd2+ and Pb2+ ions onto mango stone and cocoa pod waste: kinetic and equilibrium studies. Sci. Res. Essays 7, 1614–1629 (2012).
CAS  Article  Google Scholar 

51.
Adhiambo, O.R., Lusweti, K.J. & Morang’a, G.Z. Biosorption of Pb2+ and Cr2+ Using Moringa oleifera and their adsorption isotherms. Sci. J. Anal. Chem., 3, 100–108 (2015).

52.
Ofomaja, A. E., Naidoo, E. B. & Modise, S. J. Biosorption of copper(II) and lead(II) onto potassium hydroxide treated pine cone powder. J. Environ. Manag. 91, 1674–1685 (2010).
CAS  Article  Google Scholar 

53.
Min, S. H., Han, J. S., Shin, E. W. & Park, J. K. Improvement of cadmium ion removal by base treatment of juniper fiber. Water Res. 38, 1289–1295 (2004).
CAS  PubMed  Article  Google Scholar 

54.
Kapoor, A. & Viraraghavan, T. Heavy metal biosorption sites in Aspergillus Niger. Bioresour. Technol. 61, 221–227 (1997).
CAS  Article  Google Scholar 

55.
Vijayaraghavan, K. & Yun, Y. S. Utilization of fermentation waste (Corynebacterium glutamicum) for biosorption of reactive black 5 from aqueous solution. J. Hazard. Mater. 141, 45–52 (2007).
CAS  PubMed  Article  Google Scholar 

56.
Alslaibi, T.M., Abustan, I., Ahmad, M.A. & Abu Foul, A. Comparative studies on the olive stone activated carbon adsorption of Zn2+, Ni2+, and Cd2+from synthetic wastewater. Desalin. Water Treat., 54, 166–177 (2015).

57.
Papageorgiou, S. K. et al. Heavy metal sorption by calcium alginate beads from Laminaria digitata. J. Hazard. Mater. 137, 1765–1772 (2006).
CAS  PubMed  Article  Google Scholar 

58.
Usman, A. R. A. The relative adsorption selectivities of Pb, Cu, Zn, Cd and Ni by soils developed on shale in New Valley Egypt. Geoderma 144, 334–343 (2008).
ADS  CAS  Article  Google Scholar 

59.
Gilbert, U. A., Emmanuel, I. U., Adebanjo, A. A. & Olalere, G. A. Biosorptive removal of Pb2+ and Cd2+ onto novel biosorbent: defatted Carica papaya seeds. Biomass Bioenergy 35, 2517–2525 (2011).
Article  CAS  Google Scholar 

60.
Jimoh, T. O., Yisa, J., Ajai, A. I. & Musa, A. Kinetics and thermodynamics studies of the biosorption of Pb(II), Cd(II) and Zn(II) ions from aqueous solution by sweet orange (Citrus sinensis) seeds. Int. J. Mod. Chem. 4, 19–37 (2013).
CAS  Google Scholar 

61.
Shawabkeh, R., Al-Harahsheh, A., Hami, M. & Khlaifat, A. Conversion of oil shale ash into zeolite for cadmium and lead removal from wastewater. Fuel 83, 981–985 (2004).
CAS  Article  Google Scholar 

62.
Politzer, P. & Murray, J.S. Molecular electrostatic potentials. In Concepts and Applications, (Theoretical and Computational Chemistry), 1st edn.; Murray, J.S., Sen, K., Eds.; Elsevier: Amsterdam, 3, 649–660 (1996).

63.
Ibrahim, A., Elhaes, H., Meng, F. & Ibrahim, M. Effect of hydration on the physical properties of glucose. Biointerface Res. Appl. Chem. 8, 4114–4118 (2019).
Google Scholar 

64.
Ibrahim, A., Elhaes, H., Ibrahim, M., Yahia, I. S. & Zahran, H. Y. Molecular modeling analyses for polyvinylidene X (X=F, Cl, Br and I). Biointerface Res. Appl. Chem. 9, 3890–3893 (2019).
CAS  Article  Google Scholar 

65.
Ezzat, H. et al. Mapping the molecular electrostatic potential of carbon nanotubes. Biointerface Res. Appl. Chem. 8, 3539–3542 (2018).
CAS  Google Scholar 

66.
Msaada, A. et al. Industrial wastewater decolorization by activated carbon from Ziziphus lotus. Desalin. Water Treat. 126, 296–305 (2018).
Article  CAS  Google Scholar 

67.
Msaad, A., Belbahloul, M., El Hajjaji, S. & Zouhri, A. Comparison of novel Ziziphus lotus adsorbent and industrial carbon on methylene blue removal from aqueous solutions. Water Sci. Technol. 78(10), 2055–2063 (2018).
CAS  PubMed  Article  Google Scholar 

68.
Msaad, A., Belbahloul, M., El Hajjaji, S., Zouhri, A. Synthesis of H3PO4 activated carbon from Ziziphus lotus (Z. mauritiana) leaves: optimization using RSM and cationic dye adsorption. Desalin. Water Treat. 153, 288–299 (2019).
CAS  Article  Google Scholar  More

1.
Dingle, H. & Drake, A. What is migration?. Bioscience 57, 113–121 (2007).
Article  Google Scholar 
2.
Dingle, H. Migration: The Biology of Life on the Move (Oxford University Press, Oxford, 2014).
Google Scholar 

3.
Chapman, J. W., Reynolds, D. R. & Wilson, K. Long-range seasonal migration in insects: mechanisms, evolutionary drivers and ecological consequences. Ecol. Lett. 18, 287–302 (2015).
PubMed  Article  Google Scholar 

4.
Maiga, I. H., Lecoq, M. & Kooyman, C. Ecology and management of the Senegalese grasshopper Oedaleus senegalensis (Krauss 1877) (Orthoptera: Acrididae) in West Africa. Ann. Soc. Entomol. Fr. 44, 271–288 (2008).
Article  Google Scholar 

5.
Glick, P. A. The distribution of insects, spiders, and mites in the air. United States Department of Agriculture, Technical Bulletin 673, (1939).

6.
Rainey, R. C. Migration and Meteorology (Clarendon Press, Oxford, 1989).
Google Scholar 

7.
Cheke, R. A. et al. A migrant pest in the Sahel: the Senegalese grasshopper Oedaleus senegalensis. Philos. Trans. R. Soc. B 328, 539–553 (1990).
ADS  Google Scholar 

8.
Chapman, J. W., Reynolds, D. R. & Smith, A. D. Migratory and foraging movements in beneficial insects: a review of radar monitoring and tracking methods. Int. J. Pest Manag. 50, 225–232 (2004).
Article  Google Scholar 

9.
Reynolds, D. R., Chapman, J. W. & Harrington, R. The migration of insect vectors of plant and animal viruses. Adv. Virus Res. 67, 453–517 (2006).
CAS  PubMed  Article  Google Scholar 

10.
Garms, R., Walsh, J. F. & Davies, J. B. Studies on the reinvasion of the Onchocerciasis Control Programme in the Volta River basin by Simulium damnosum s.l. with emphasis on the sout-western areas. Tropenmed. Parasitol. 30, 345–362 (1979).
CAS  PubMed  Google Scholar 

11.
Sellers, R. F. Weather, host and vector–their interplay in the spread of insect-borne animal virus diseases. J. Hyg. (Lond) 85, 65–102 (1980).
CAS  Article  Google Scholar 

12.
Ming, J. et al. Autumn southward ‘return’ migration of the mosquito Culex tritaeniorhynchus in China. Med. Vet. Entomol. 7, 323–327 (1993).
CAS  PubMed  Article  Google Scholar 

13.
Ritchie, S. A. & Rochester, W. Wind-blown mosquitoes and introduction of Japanese encephalitis into Australia. Emerg. Infect. Dis. 7, 900–903 (2001).
CAS  PubMed  PubMed Central  Article  Google Scholar 

14.
Eagles, D., Walker, P. J., Zalucki, M. P. & Durr, P. A. Modelling spatio-temporal patterns of long-distance Culicoides dispersal into northern Australia. Prev. Vet. Med. 110, 312–322 (2013).
CAS  PubMed  Article  Google Scholar 

15.
Huestis, D. L. et al. Windborne long-distance migration of malaria mosquitoes in the Sahel. Nature 574, 404–408 (2019).
CAS  PubMed  Article  Google Scholar 

16.
Green, K. The transport of nutrients and energy into the Australian Snowy Mountains by migrating bogong moth Agrotis infusa. Austral. Ecol. 36, 25–34 (2011).
Article  Google Scholar 

17.
Landry, J.-S. & Parrott, L. Could the lateral transfer of nutrients by outbreaking insects lead to consequential landscape-scale effects?. Ecosphere 7, e01265 (2016).
Article  Google Scholar 

18.
Stefanescu, C. et al. Multi-generational long-distance migration of insects: studying the painted lady butterfly in the Western Palaearctic. Ecography (Cop.) 36, 474–486 (2013).
Article  Google Scholar 

19.
Chapman, J. W. et al. Seasonal migration to high latitudes results in major reproductive benefits in an insect. Proc. Natl. Acad. Sci. 109, 14924–14929 (2012).
ADS  CAS  PubMed  Article  Google Scholar 

20.
Chapman, J. W. et al. Wind selection and drift compensation optimize migratory pathways in a high-flying moth. Curr. Biol. 18, 514–518 (2008).
CAS  PubMed  Article  Google Scholar 

21.
Hallworth, M. T., Marra, P. P., McFarland, K. P., Zahendra, S. & Studds, C. E. Tracking dragons: stable isotopes reveal the annual cycle of a long-distance migratory insect. Biol. Lett. 14, 20180741 (2018).
PubMed  PubMed Central  Article  Google Scholar 

22.
Hu, G. et al. Mass seasonal bioflows of high-flying insect migrants. Science (80-.) 354, 1584–1587 (2016).
ADS  CAS  Article  Google Scholar 

23.
Wotton, K. R. et al. Mass seasonal migrations of hoverflies provide extensive pollination and crop protection services. Curr. Biol. 29, 2167-2173.e5 (2019).
CAS  PubMed  Article  Google Scholar 

24.
Drake, V. A. & Reynolds, D. R. Radar Entomology: Observing Insect Flight and Migration (CAB International, Wallingford, 2012).
Google Scholar 

25.
Holland, R. A. How and why do insects migrate?. Science (80-.) 313, 794–796 (2006).
ADS  CAS  Article  Google Scholar 

26.
Faiman, R. et al. Marking mosquitoes in their natural larval sites using 2 H-enriched water: a promising approach for tracking over extended temporal and spatial scales. Methods Ecol. Evol. 10, 1274–1285 (2019).
PubMed  PubMed Central  Article  Google Scholar 

27.
Cheke, R. A. & Tratalos, J. A. Migration, patchiness, and population processes illustrated by two migrant pests. Bioscience 57, 145–154 (2007).
Article  Google Scholar 

28.
Lecoq, M. Recent progress in Desert and Migratory Locust management in Africa. Are preventative actions possible ? 10, 277–291 (2001). https://doi.org/https://doi.org/10.1665/1082-6467(2001)010[0277:RPIDAM]2.0.CO;2.

29.
Rose, D. J. W., Dewhurst, C. F. & Page, W. W. African Armyworm Handbook: The Status, Biology, Ecology, Epidemiology and Management of Spodoptera exempta (Lepidoptera: Noctuidae) (University of Greenwich, Natural Resources Institute, 2000).
Google Scholar 

30.
Gebreyes, W. A. et al. The global one health paradigm: challenges and opportunities for tackling infectious diseases at the human, animal, and environment interface in low-resource settings. PLoS Negl. Trop. Dis. 8, e3257 (2014).
PubMed  PubMed Central  Article  Google Scholar 

31.
Nicholson, S. E. The West African Sahel: a review of recent studies on the rainfall regime and its interannual variability. ISRN Meteorol. 2013, 32 (2013).
Article  Google Scholar 

32.
Chapman, J. W., Reynolds, D. R., Smith, A. D., Smith, E. T. & Woiwod, I. P. An aerial netting study of insects migrating at high altitude over England. Bull. Entomol. Res. 94, 123–136 (2004).
CAS  PubMed  Article  Google Scholar 

33.
Drake, V. A. & Gatehouse, A. G. Insect Migration: Tracking Resources Through Space and Time (Cambridge University Press, Cambridge, 1995).
Google Scholar 

34.
Southwood, T. R. E. Migration of terrestrial arthropods in relation to habitat. Biol. Rev. 37, 171–211 (1962).
Article  Google Scholar 

35.
Frank, J. & Kanamitsu, K. Paederus, sensu lato (Coleoptera: Staphilinidae): natural history and medical importance. J. Med. Entomol. 24, 155–191 (1987).
CAS  PubMed  Article  Google Scholar 

36.
Vanhecke, C., Le Gall, P. & Gaüzère, B. A. Vesicular contact dermatitis due to Paederus in Cameroon and review of the literature. Bull. la Soc. Pathol. Exot. 108, 328–336 (2015).
CAS  Article  Google Scholar 

37.
Duviard, D. Migrations of Dysdercus spp (Hemiptera: Pyrrhocoridae) related to movements of the Inter-Tropical Convergence Zone in West Africa. Bull. Entomol. Res. 67, 185 (1977).
Article  Google Scholar 

38.
Dao, A. et al. Signatures of aestivation and migration in Sahelian malaria mosquito populations. Nature 516, 387–390 (2014).
ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

39.
Garrett-Jones, C. The possibility of active long-distance migrations by Anopheles pharoensis Theobald. Bull. World Health Organ. 27, 299–302 (1962).
CAS  PubMed  PubMed Central  Google Scholar 

40.
Faiman, R. et al. Quantifying flight aptitude variation in wild A. gambiae s.l. in order to identify long-distance migrants. Malar. J. DOI: https://doi.org/10.1186/s12936-020-03333-2 (2020).

41.
Morkel, C. & Jacobs, D. H. New records of stilt bugs (Insecta, Heteroptera, Berytidae) from the Afrotropical region, with distributional and ecological notes. Andrias 20, 153–173 (2014).
Google Scholar 

42.
Hocking, B. The intrinsic range and speed of flight of insects. Trans. R. Entomol. Soc. Lond. 104, 223–345 (1953).
Google Scholar 

43.
Snow, W. F. Field estimates of the flight speed of some West African mosquitoes. Ann. Trop. Med. Parasitol. 74, 239–242 (1980).
CAS  PubMed  Article  Google Scholar 

44.
Lee, D.-H. & Leskey, T. C. Flight behavior of foraging and overwintering brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae). Bull. Entomol. Res. 105, 566–573 (2015).
PubMed  PubMed Central  Article  Google Scholar 

45.
Taylor, R. A. J., Bauer, L. S., Poland, T. M. & Windell, K. N. Flight performance of Agrilus planipennis (Coleoptera: Buprestidae) on a flight mill and in free flight. J. Insect Behav. 23, 128–148 (2010).
Article  Google Scholar 

46.
Cooter, R. J., Winder, D. & Chancellor, T. C. Tethered flight activity of Nephotettix virescens (Hemiptera: Cicadellidae) in the Philippines. Bull. Entomol. Res. 90, 49–55 (2000).
CAS  PubMed  Article  Google Scholar 

47.
Briegel, H., Knüsel, I. & Timmermann, S. E. Aedes aegypti: size, reserves, survival, and flight potential. J. Vector Ecol. Ecol. 26, 21–31 (2001).
CAS  Google Scholar 

48.
Kaufmann, C. & Briegel, H. Flight performance of the malaria vectors Anopheles gambiae and Anopheles atroparvus. J. Vector Ecol. 29, 140–153 (2004).
PubMed  Google Scholar 

49.
Reynolds, D. R. et al. Radar studies of the vertical distribution of insects migrating over southern Britain: the influence of temperature inversions on nocturnal layer concentrations. Bull. Entomol. Res. 95, 259–274 (2005).
CAS  PubMed  Article  Google Scholar 

50.
Wood, C. R. et al. Flight periodicity and the vertical distribution of high-altitude moth migration over southern Britain. Bull. Entomol. Res. 99, 525–535 (2009).
CAS  PubMed  Article  Google Scholar 

51.
Reynolds, D. R. & Riley, J. R. A migration of grasshoppers, particularly Diabolocatantops axillaris (Thunberg) (Orthoptera: Acrididae), in the West African Sahel. Bull. Entomol. Res. 78, 251–271 (1988).
Article  Google Scholar 

52.
Madougou, S., Saïd, F., Campistron, B., Lothon, M. & Kebe, C. Results of UHF radar observation of the nocturnal low-level jet for wind energy applications. Acta Geophysica 60, (2012).

53.
Fiedler, S., Schepanski, K., Heinold, B., Knippertz, P. & Tegen, I. Climatology of nocturnal low-level jets over North Africa and implications for modeling mineral dust emission. J. Geophys. Res. Atmos. 118, 6100–6121 (2013).
ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

54.
Åkesson, S., Bianco, G. & Hedenström, A. Negotiating an ecological barrier: crossing the Sahara in relation to winds by common swifts. Philos. Trans. R. Soc. B-Biological Sci. Ser. B, Biol. Sci. 371, 20150393 (2016).

55.
Åkesson, S., Klaassen, R., Holmgren, J., Fox, J. W. & Hedenström, A. Migration routes and strategies in a highly aerial migrant, the common swift Apus apus, revealed by light-level geolocators. PLoS ONE 7, e41195 (2012).
ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

56.
Jackson, H. A review of foraging and feeding behaviour, and associated anatomical adaptations, Afrotropical nightjars. Ostrich 74, 187–204 (2003).
Article  Google Scholar 

57.
Fenton, M. B. & Griffin, D. R. High-altitude pursuit of insects by echolocating bats. J. Mammal. 78, 247–250 (1997).
Article  Google Scholar 

58.
Pedgley, D. E., Reynolds, D. R. & Tatchell, G. M. Long-range insect migration in relation to climate and weather: Africa and Europe. in Insect Migration: Tracking Resources Through Space and Time (eds. Drake, V. A. & Gatehouse, A. G.) 3–30 (Cambridge University Press, Cambridge, 1995).

59.
Schneider, T., Bischoff, T. & Haug, G. H. Migrations and dynamics of the intertropical convergence zone. Nature 513, 45–53 (2014).
ADS  CAS  PubMed  Article  Google Scholar 

60.
Persistence in the Sahel. Huestis, D. L. & Lehmann, T. Ecophysiology of Anopheles gambiae s.l. Infect. Genet. Evol. 28, 648–661 (2014).
Article  Google Scholar 

61.
Yaro, A. S. et al. Dry season reproductive depression of Anopheles gambiae in the Sahel. J. Insect Physiol. 58, 1050–1059 (2012).
CAS  PubMed  PubMed Central  Article  Google Scholar 

62.
Krajacich, B. J. et al. Induction of long-lived potential aestivation states in laboratory An. gambiae mosquitoes. bioRxiv (2020). https://doi.org/10.1101/2020.04.14.031799

63.
della Torre, A. et al. Speciation within Anopheles gambiae–the glass is half full. Science (80-. ). 298, 115–117 (2002).

64.
della Torre, A., Tu, Z. & Petrarca, V. On the distribution and genetic differentiation of Anopheles gambiae s.s. molecular forms. Insect Biochem. Mol. Biol. 35, 755–769 (2005).

65.
Neafsey, D. E. et al. Mosquito genomics. Highly evolvable malaria vectors: the genomes of 16 Anopheles mosquitoes. Science (80-. ). 347, 1258522 (2015).

66.
Chapman, J. W. et al. Flight orientation behaviors promote optimal migration trajectories in high-flying insects. Science (80-. ). 327, 682–685 (2010).

67.
Lehmann, T. et al. Aestivation of the African Malaria Mosquito, Anopheles gambiae in the Sahel. Am. J. Trop. Med. Hyg. 83, 601–606 (2010).
PubMed  PubMed Central  Article  Google Scholar 

68.
Huestis, D. L. et al. Seasonal variation in metabolic rate, flight activity and body size of Anopheles gambiae in the Sahel. J Exp Biol 215, 2013–2021 (2012).
PubMed  PubMed Central  Article  Google Scholar 

69.
Lehmann, T. et al. Tracing the origin of the early wet-season Anopheles coluzzii in the Sahel. Evol. Appl. 10, 704–717 (2017).
CAS  PubMed  PubMed Central  Article  Google Scholar 

70.
Gelaro, R. et al. The modern-era retrospective analysis for research and applications, version 2 (MERRA-2). J. Clim. 30, 5419–5454 (2017).
ADS  PubMed  Article  Google Scholar 

71.
Taylor, L. R. Insect migration, flight periodicity and the Boundary Layer. J. Anim. Ecol. 43, 225–238 (1974).
Article  Google Scholar 

72.
Chapman, J. W., Drake, V. A. & Reynolds, D. R. Recent insights from radar studies of insect flight. Annu. Rev. Entomol. 56, 337–356 (2011).
CAS  PubMed  Article  Google Scholar 

73.
SAS Inc., I. SAS for Windows Version 9.4. (2012).

74.
Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer-Verlag, New York, 2016).
Google Scholar  More

Systematic paleontology
Frondicuniculum ichnogen. nov.
Etymology. Classical Latin: frons -dis, a leaf, leafy twig or foliage; and cuniculum-i, meaning a mine, underground passage, hole or pit.
Type ichnospecies. Frondicuniculum lineacurvum ichnosp. nov.
Diagnosis. Elongate-ellipsoidal blotch mines occurring on broadleaved, parallel veined conifer leaves. Long axes of the mines are parallel to leaf venation. Frass, when present, is densely packed, composed of spheroidal pellets surrounded by amorphous matter, often positioned along one margin of the mine. Leaf veins within mines are distorted.
Frondicuniculum lineacurvum ichnosp. nov.
Etymology. Classical Latin: linea-e, a string, linen thread, or drawn line; and curvus–a –um, bent, bowed, arched, or curved.
Holotype. MPEF-Pb 6336 (Fig. 1d–f and Supplementary Fig. 3a–e), Laguna del Hunco quarry LH610, early Eocene, Chubut Province, Argentina.
Paratypes. MPEF-Pb 3160 (Laguna del Hunco quarry LH6, Supplementary Fig. 3f), USNM 545226 (Río Pichileufú historical collection48, Fig. 1g, h and Supplementary Fig. 4a, b).
Diagnosis. As for the genus, with smooth, linear to gently curving mine margins.
Description. An elongate-ellipsoidal blotch mine positioned along leaf margin, long axis parallel to leaf veins, mine margins well defined, linear to gently curving. Mine dimensions 7.2–50.0 mm long by 2.0–10.0 mm wide. Frass, when present, composed of spherical or hemispherical pellets measuring 0.04–0.12 mm in diameter and surrounded by dark, amorphous matter. Frass pellets mostly positioned near mine margin and may be replaced by surrounding amber with original frass material not preserved. Reaction rim 0.1–0.3 mm wide present at contact between mine margins and surrounding leaf tissue. Individual specimen descriptions of holotype and paratypes provided in Supplementary Note 1.
Occurrence. Huitrera Formation, Laguna del Hunco (early Eocene, Chubut Province, Argentina) and Río Pichileufú (middle Eocene, Río Negro Province, Argentina), on host plant Agathis zamunerae Wilf.
Repositories. Museo Paleontológico Egidio Feruglio, Trelew, Chubut, Argentina (MPEF-Pb), and Smithsonian Institution, National Museum of Natural History (USNM).
Frondicuniculum flexuosum ichnosp. nov.
Etymology. Classical Latin: flexuosus –a –um, full of winding turns, bent, or crooked.
Holotype. MPEF-Pb 5970 (Fig. 1a–c and Supplementary Fig. 2a–c), Palacio de los Loros 2 (PL2)42, Salamanca Formation, early Paleocene, Chubut Province, Argentina.
Paratypes. MPEF-Pb 5960 (Supplementary Fig. 2d, e), MPEF-Pb 6007 (Supplementary Fig. 2f, g), MPEF-Pb 6001 (Supplementary Fig. 2h–j), all from the PL2 locality.
Diagnosis. As for the genus, with wavy mine margins.
Description. An elongate-ellipsoidal blotch mine with gentle to strongly undulatory margins having a raised, wrinkly appearance. Mine positioned along leaf margin, long axis of the mine parallel to leaf veins. Mine dimensions 11.4–35.2 mm long by 1.2–9.4 mm wide. Frass, when present, composed of spheroidal pellets measuring ca. 0.1 mm in diameter and surrounded by smaller fragments of amorphous frass. Frass distributed throughout mine or positioned laterally near one margin of the mine. Mine margins 0.2–8.0 mm wide. Individual specimen descriptions of holotype and paratypes provided in Supplementary Note 1.
Occurrence. Palacio de los Loros 2 locality; Salamanca Formation, early Paleocene; Chubut Province, Argentina, on host plant Agathis immortalis Escapa, Iglesias, Wilf, Catalano, Caraballo et Cúneo.
Repository. Museo Paleontológico Egidio Feruglio, Trelew, Chubut, Argentina (MPEF-Pb).
Remarks
For clarity, we note that the new zoological typifications and identifications assigned here refer only to the insect-damaged areas (i.e., trace fossils) of the cited fossil material, which often has separate botanical typification and identification under the same repository numbers as defined by Wilf et al.22 for Agathis zamunerae and Escapa et al.7 for Agathis immortalis. Morphologically similar, elongate-ellipsoidal blotch mines are associated with Agathis at PL2 (early Paleocene, 4 specimens), LH (early Eocene, 2 specimens), and RP (early/middle Eocene, 1 specimen), as well as Cretaceous cf. Agathis (see next paragraph), with minor differences in their margin structure. Frondicuniculum flexuosum mines have undulatory, wrinkled margins (Fig. 1a, c, and Supplementary Fig. 2a–j), whereas F. lineacurvum mines (Fig. 1d–h and Supplementary Figs. 3a–f, 4a, b) have smooth, gently curving margins. However, the overall shape, position on leaves, frass characters, and persistence through ca. 18 myr on the same host genus from the same region suggest that the mines were made by similar, probably closely related leaf-mining insects.
A blotch mine positioned along the central axis of a cf. Agathis leaf from the Maastrichtian Lefipán Formation is characterized by an elongate-ellipsoidal shape with its long axis parallel to the leaf veins and smooth, gently curved margins (Fig. 1i and Supplementary Fig. 1a–c). The mine lacks frass, which may be a preservational effect, and otherwise could be the same as Frondicuniculum lineacurvum. Because of the preservation and because there is only one specimen, or possibly two (Supplementary Fig. 1d), we did not assign a formal name to this specimen. However, the overall similarity of Cretaceous and Paleocene blotch mines on Agathis (elongate-elliposidal shape, smooth margins, distorted leaf veins) is noteworthy as the first likely evidence of a Cretaceous-Paleogene (K-Pg) boundary crossing leaf-mine association on closely related plants. Until now, no evidence has been found of surviving K-Pg leaf-mine associations within regional Maastrichtian and Danian floras anywhere in the world46,49,50.
Another probable blotch-mine type from LH and RP (Eocene) has a linear trajectory and is oriented parallel to the leaf veins, exhibiting breached epidermal tissue (DT251; Fig. 2a, b and see Supplementary Note 1 for detailed descriptions). The putative mines have a similar appearance to slot feeding characterized by elongate holes, although their smooth, gently curving margins suggest a leaf-mining origin. Some of these mine-like structures are flanked by flaps of epidermal tissue, attributable to breaching of the tissue due to environmental factors such as in vivo abrasion (Fig. 2a). The margins along the field of damage are smooth and sometimes influenced by leaf veins. We found similar damage as possible mines on modern Australian Agathis robusta (Fig. 2c and Supplementary Fig. 5m, Supplementary Note 1), featuring an elongate-ellipsoidal shape oriented parallel to the leaf veins. Like the fossils, the epidermal tissue of the extant mines is often breached (Fig. 2c and Supplementary Fig. 5m), leaving flaps of unconsumed tissue surrounded by a thin, darkened rim of reaction tissue.
Fig. 2: External foliage feeding, blotch and serpentine mining, galling, and possible armored scale insect remains (Diaspididae) on fossil and extant Agathis.

a Putative blotch mine, or slot feeding, characterized by parallel sides and flaps of necrotic tissue on A. zamunerae (early Eocene, LH13, MPEF-Pb 6361). b Elongate blotch mine with breached epidermal tissue and thickened reaction rim on A. zamunerae (early middle Eocene, RP, USNM 545227). c Blotch mine, or possible slot feeding, flanked by flap of epidermal tissue on A. robusta (Queensland, Australia, (A.K. Irvine 00417 (A)). d Linear serpentine mines following leaf venation on cf. Agathis (latest Cretaceous, DT139; MPEF-Pb 9836). e Detail of frass trail in d. f Semicircular excision into the leaf margin on A. immortalis (Danian, PL2, MPEF-Pb 6091). g Shallow excision into the leaf margin with vein stringers on A. zamunerae (early Eocene, LH13, MPEF-Pb 6361). h Two adjacent excisions into the leaf margin on A. zamunerae (early/middle Eocene, RP, BAR 5002). i Two adjacent excisions into the leaf margin of A. moorei (New Caledonia, E 00106192). j Ellipsoidal gall with thickened walls surrounding unthickened epidermal tissue on A. immortalis (Danian, PL2, MPEF-Pb 9767). k Ellipsoidal gall with circular exit hole on A. ovata (New Caledonia, E 00399687). l Possible armored scale cover (Diaspididae) with concentric growth rings on A. immortalis (Danian, PL2, MPEF-Pb 5996). m Possible diaspidid scale cover on A. zamunerae, under epifluorescence (early Eocene, LH27, MPEF-Pb 6383). n Possible diaspidid scale covers on A. zamunerae, under epifluorescence (early/middle Eocene, RP, USNM 545228). o Possible diaspidid scale cover with concentric growth rings indicating two larval and an adult growth stage on A. zamunerae, under epifluorescence (middle Eocene, RP, USNM 545228). p Diaspidid scale insects that induced pit galls on A. macrophylla (Fiji, GH 01153259). q Rust fungus (Pucciniales) with aecia on a circular spot on A. zamunerae (early Eocene, LH06, MPEF-Pb 6303). r Kauri rust (Aecidium fragiforme) on A. macrophylla (Vanuatu, S.F. Kajewski 282 (K)).

Full size image

Only two extant leaf-mining insects have been documented in association with Agathis (Supplementary Data 1), both on A. australis of New Zealand, although their mines are not similar to the fossils. Larvae of the leaf blotch-miner moth Parectopa leucocyma (Lepidoptera: Gracillariidae) initially form small blotch mines that transition to linear epidermal mines and then galls39. Microlamia pygmaea, a longhorn beetle (Coleoptera: Cerambycidae), mines dead leaves on fallen branches51. In our survey of extant Agathis, we found numerous examples of blotch mines similar to our fossils on six host species that span much of the modern range of the genus (Fig. 1j–m, Supplementary Fig. 5a–f, Supplementary Note 1). The extant blotch mines, previously undocumented to our knowledge, are typically elongate-ellipsoidal and exhibit many similarities to the fossils, suggesting geologically long-term behaviors with origins in the late Mesozoic and early Cenozoic. Most mine trajectories occur along the leaf margins (Fig. 1j–m), although some course along the central axes of leaves (Supplementary Fig. 5c). The long axes of the extant blotch mines are parallel to leaf venation (Fig. 1j–m) as in the fossils. Margins of the mines are smooth to wavy.
In order to assess potential convergence of leaf mine morphologies associated with related conifers that have similar leaf architecture to Agathis, we also compared extant mines on Araucaria (Araucariaceae) and members of the Podocarpaceae family, including Nageia, Afrocarpus, Sundacarpus, and Podocarpus. Araucarivora gentilii Hodges (Elachistidae) caterpillars mine leaves of Araucaria araucana in Argentina and Chile52. Mines begin with a short serpentine phase and then expand into a raised, circular to polylobate blotch mine. A circular exit hole is typically positioned near the margin of the blotch mine. The fossil Agathis blotch mines (Fig. 1a–i and Supplementary Figs. 1–4) differ in that they are elongate and lack a serpentine phase. We did not find any other blotch mine morphologies on Araucaria herbarium specimens throughout the range of the genus (parts of South America and Australasia). Three leaf-mining taxa have been described on Podocarpus. Phyllocnistis podocarpa (Lepidoptera: Gracillariidae) larvae mine Podocarpus macrophyllus leaves in Japan, creating serpentine mines with overlapping paths that often form into a blotch, although their zigzag frass trail is distinct from the fossil Agathis blotch mines53. In New Zealand, Podocarpus totara hosts two leaf miners, including Chrysorthenches polita (Lepidoptera: Glyphipterigidae), whose mines have not been described54, and Peristoreus flavitarsis (Coleoptera: Curculionidae)55. The mines of Peristoreus flavitarsis are a possible extant analog to the fossil Agathis mines, in addition to similar mines we found on extant Agathis (Fig. 1j–m and Supplementary Fig. 5). The mines are full depth and typically span the width of the leaf. Frass pellets are often deposited along portions of the mine margin at the edge of the leaf. Individual larvae make mines on multiple leaves. Before pupating in the soil or litter, the larva chews a circular hole through the epidermis on the abaxial side of the leaf55. We found other putative blotch mines on herbarium sheets of Podocarpus with similar morphologies to those on extant and fossil Agathis, including on Podocarpus ingensis from Bolivia, Podocarpus oleifolius from Colombia, and Podocarpus urbanii from Jamaica. We did not find any comparable mines on herbarium specimens of Afrocarpus, Nageia, or Sundacarpus.
Leaf mines have been recognized on other broadleaved, parallel-veined gymnosperms from the Mesozoic, although Frondicuniculum is distinguished from all the Mesozoic examples by its blotch morphology and lack of a serpentine phase. Similar to our Cretaceous specimens (Fig. 2d, e, and Supplementary Fig. 1e, f), unnamed mines on the voltzialean conifer Heidiphyllum elongatum, from the Late Triassic (Carnian) of the Karoo Basin in South Africa56,57, exhibit an elongate, parallel-sided, rectilinear path with spheroidal pellets often deposited in an approximate meniscate pattern. Triassohyponomus dinmorensis mines, also on H. elongatum but from the Blackstone Formation (Middle Triassic) in Australia58, are serpentine and have an extensive, tightly sinusoidal to meniscate pattern. Fossafolia offae on Liaoningocladus boii from the Early Cretaceous Yixian Formation of northeast China begins as a serpentine mine with an intestiniform frass trail and transitions to a blotch phase59. The blotch mines on Patagonian fossil and living Old World Agathis therefore appear to represent part of a suite of leaf mining insects of uncertain interrelationships that has colonized parallel-veined, broadleaved seed plants since the Mesozoic, but which nevertheless are distinct from the Mesozoic examples in producing the blotch-mine morphology with no serpentine phase.
Additional damage diversity
In addition to leaf mines, fossil and extant Agathis are associated with a variety of other insect feeding types (Table 1), which we sketch here while details are being prepared separately. External foliage feeding includes small circular holes (DT1, DT2; Table 1), semicircular excisions into leaf margins (DT12; Fig. 2f–h), and swaths of surface feeding (DT29). A similar spectrum of damage is found on extant Agathis throughout its range (Fig. 2i). However, many types of external foliage-feeding damage can be made by a variety of insects with mandibulate mouthparts across several taxonomic orders60, and their presence at multiple fossil and modern sites does not necessarily indicate that the same suite of closely-related insect groups produced the damage.
Table 1 Insect damage types on fossil and extant Agathis.
Full size table

Four gall DTs are associated with fossil Agathis in Patagonia, including nondiagnostic, dark circular galls (DT32; Lef and LH), circular galls with a nonhardened center surrounded by a thickened outer rim (DT11; PL2), and columnar galls (DT116; PL2). Moreover, at PL2, A. immortalis is associated with ellipsoidal galls bearing a thickened outer wall surrounding epidermal tissue with files of cells. The center of each gall is marked by a circular dot representing the central chamber or exit hole (Fig. 2j). The fossils resemble undescribed ellipsoidal galls on A. ovata from New Caledonia, which are characterized by a raised rim of thickened tissue surrounding a flat, epidermal surface with a circular exit hole (Fig. 2k). The only previously documented galling insect on extant Agathis is Conifericoccus agathidis (Hemiptera: Margarodidae), the kauri coccid, whose second-instar nymphs induce blister galls that have caused extensive defoliation of Agathis robusta in Australia61. Nevertheless, we found abundant and diverse gall morphologies on extant Agathis (Fig. 2k and Table 1).
Possible covers of female armored scale insects (Diaspididae) occur on Agathis at PL2 (Fig. 2l), LH (Fig. 2m), and RP (Fig. 2n, o). At PL2, the covers are found on leaves and a cone scale7. The dorsal covers are characterized by concentric growth rings made during the construction of the cover through two instars and an adult phase (Fig. 2l–o). Ventral covers surround the dorsal covers (Fig. 2m) and, in some cases, appear to be deeply set in the leaf tissue and leave a columnar or circular pit when detached. We caution that other interpretations of these structures remain possible because some of their features are not present on extant diaspidid covers (off-center indent or hole on dorsal covers) or are atypical (ventral cover structure surrounding dorsal cover; only adult female covers are present). The possible scale covers, including the-off center indent, are very similar to structures assigned to Diaspididae from the Late Cretaceous of New Zealand and Australia62, and comparable scale covers are associated with angiosperm leaves from the Eocene of Germany63 and Miocene of New Zealand64. On extant Agathis, diaspidid scales previously have been documented on three species in New Zealand and Australia (Supplementary Data 1). We found diaspidids on Agathis herbarium specimens from New Caledonia and Fiji, including an unidentified diaspidid species that induced pit galls on A. macrophylla from Fiji (Fig. 2p).
A probable rust fungus (Pucciniales), characterized by rings of circular to oval aecia on a circular gall, is associated with Agathis zamunerae at LH (Fig. 2q). Two species of rust fungi in the genus Aecidium parasitize extant Agathis: Aecidium fragiforme from Oceania and Malesia and Aecidium balansae in New Caledonia (Fig. 2r)40,65. Aecidium on extant Agathis produces galls covered in yellow aecia (Fig. 2p). The very similar morphologies of the fossil and extant rust on Agathis suggest long-term, persistent associations reaching back to at least the early Eocene. More

1.
Moberg, F. & Folke, C. Ecological goods and services of coral reef ecosystems. Ecol. Econ. 29, 215–233. https://doi.org/10.1016/s0921-8009(99)00009-9 (1999).
Article  Google Scholar 
2.
Lai, S., Loke, L. H. L., Hilton, M. J., Bouma, T. J. & Todd, P. A. The effects of urbanisation on coastal habitats and the potential for ecological engineering: a Singapore case study. Ocean Coast Manage. 103, 78–85. https://doi.org/10.1016/j.ocecoaman.2014.11.006 (2015).
Article  Google Scholar 

3.
Ng, C. S. L., Toh, T. C. & Chou, L. M. Current status of coral reef restoration in Singapore. in Proceedings of the Asian Conference on Sustainability, Energy & the Environment, 546–558 (2013).

4.
Ng, C. S. L., Chen, D. & Chou, L. M. Hard coral assemblages on seawalls in Singapore. In Contributions to Marine Science (ed. Tan, K. S.) 75–79 (Tropical Marine Science Institute, Singapore, 2012).
Google Scholar 

5.
Horoszowski-Fridman, Y. B. & Rinkevich, B. Restoration of the animal forests: harnessing silviculture biodiversity concepts for coral transplantation. In Marine Animal Forests (ed. Rossi, S.) 1313–1335 (Springer, Cham, 2016).
Google Scholar 

6.
Ng, C. S. L. et al. Enhancing the biodiversity of coastal defence structures: transplantation of nursery-reared reef biota onto intertidal seawalls. Ecol. Eng. 82, 480–486. https://doi.org/10.1016/j.ecoleng.2015.05.016 (2015).
Article  Google Scholar 

7.
Karlson, R. H. Dynamics of Coral Communities (Kluwer Academic Publishers, Dordrecht, 2002).
Google Scholar 

8.
Glynn, P. W. & Enochs, I. C. Invertebrates and their roles in coral reef ecosystems. In Coral Reefs: An Ecosystem in Transition (eds Dubinsky, Z. & Stambler, N.) 273–325 (Springer, Dordrecht, 2010).
Google Scholar 

9.
Fong, P. & Paul, J. V. Coral reef algae: the good, the bad, and the ugly. In Coral Reefs: An Ecosystem in Transition (eds Dubinsky, Z. & Stambler, N.) (Springer, Dordrecht, 2010).
Google Scholar 

10.
Swierts, T. & Vermeij, M. J. A. Competitive interactions between corals and turf algae depend on coral colony form. PeerJ 4, e1984. https://doi.org/10.7717/peerj.1984 (2016).
CAS  Article  PubMed  PubMed Central  Google Scholar 

11.
Lang, J. C. & Chornesky, E. A. Competition between scleractinian reef corals—a review of mechanisms and effects. In Ecosystems of the World (ed. Dubinsky, Z.) 133–206 (Elsevier, Amsterdam, 1990).
Google Scholar 

12.
Tanner, J. E. Interspecific competition reduces fitness in scleractinian corals. J. Exp. Mar. Biol. Ecol. 214, 19–34. https://doi.org/10.1016/S0022-0981(97)00024-5 (1997).
Article  Google Scholar 

13.
Birrell, C. L., McCook, L. J., Willis, B. L. & Diaz-Pulido, G. A. Effects of benthic algae on the replenishment of corals and the implications for the resilience of coral reefs. Oceanogr. Mar. Biol. Ann. Rev. 46, 25–63 (2008).
Google Scholar 

14.
Connell, J. H. et al. A long-term study of competition and diversity of corals. Ecol. Monogr. 74, 179–210. https://doi.org/10.1890/02-4043 (2004).
Article  Google Scholar 

15.
Paine, R. T. Ecological determinism in the competition for space: the Robert H. MacArthur award lecture. Ecology 65, 1339–1348. https://doi.org/10.2307/1939114 (1984).
Article  Google Scholar 

16.
Buss, L. W. Competition and community organization on hard surfaces in the sea. In Community Ecology (eds Diamond, J. & Case, T. J.) (Harper and Row, New York, 1986).
Google Scholar 

17.
Chadwick, N. E. Spatial distribution and the effects of competition on some temperate scleractinia and coralliomorpharia. Mar. Ecol. Prog. Ser. 70, 39–48 (1991).
ADS  Article  Google Scholar 

18.
Romano, S. L. Long-term effects of interspecific aggression on growth of the reef-building corals Cyphastrea ocellina (Dana) and Pocilloporu damicornis (Linnaeus). J. Exp. Mar. Biol. Ecol. 140, 135–146. https://doi.org/10.1016/0022-0981(90)90087-S (1990).
Article  Google Scholar 

19.
Rinkevich, B. & Loya, Y. Intraspecific competition in a reef coral: effects on growth and reproduction. Oecologia 66, 100–105. https://doi.org/10.1007/BF00378559 (1985).
ADS  CAS  Article  PubMed  Google Scholar 

20.
Chadwick, N. E. & Morrow, K. M. Competition among sessile organisms on coral reefs. In Coral Reefs: An Ecosystem in Transition (eds Dubinsky, Z. & Stambler, N.) 347–371 (Springer, Dordrecht, 2011).
Google Scholar 

21.
Rinkevich, B. & Loya, Y. Intraspecific competitive networks in the Red Sea coral Stylophora pistillata. Coral Reefs 1, 161–172. https://doi.org/10.1007/BF00571193 (1983).
ADS  Article  Google Scholar 

22.
Leslie, P. H. On the use of matrices in certain population mathematics. Biometrika 33, 183–212 (1945).
MathSciNet  CAS  Article  Google Scholar 

23.
Connell, J. H. On the prevalence and relative importance of interspecific competition: evidence from field experiments. Am. Nat. 122, 661–669. https://doi.org/10.1086/284165 (1983).
Article  Google Scholar 

24.
Schoener, T. W. Field experiments on interspecific competition. Am. Nat. 122, 240–285. https://doi.org/10.1086/284133 (1983).
Article  Google Scholar 

25.
Barnes, R. S. K. & Hughes, R. N. An Introduction to Marine Ecology (Blackwell Scientific, Hoboken, 1988).
Google Scholar 

26.
Abelson, A. & Loya, Y. Interspecific aggression among stony corals in Eilat, Red Sea: a hierarchy of aggression ability and related parameters. Br. Mar. Sci. 65, 851–860 (1999).
Google Scholar 

27.
Tylianakis, J. M., Didham, R. K., Bascompte, J. & Wardle, D. A. Global change and species interactions in terrestrial ecosystems. Ecol. Lett. 11, 1351–1363. https://doi.org/10.1111/j.1461-0248.2008.01250.x (2008).
Article  PubMed  Google Scholar 

28.
Breeuwer, A., Heijmans, M. P. D., Robroek, B. J. M. & Berendse, F. The effect of temperature on growth and competition between Sphagnum species. Oecologia 156, 155–167. https://doi.org/10.1007/s00442-008-0963-8 (2008).
ADS  Article  PubMed  PubMed Central  Google Scholar 

29.
Edmunds, P. J. et al. Persistence and change in community composition of reef corals through present, past, and future climates. PLoS ONE 9, e107525. https://doi.org/10.1371/journal.pone.0107525 (2014).
ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

30.
Hidaka, M. & Yamazato, K. Intraspecific interactions in a scleractinian coral, Galaxea fascicularis: induced formation of sweeper tentacles. Coral Reefs 3, 77–85. https://doi.org/10.1007/BF00263757 (1984).
ADS  Article  Google Scholar 

31.
Lapid, E. D., Wielgus, J. & Chadwick-Furman, N. E. Sweeper tentacles of the brain coral Platygyra daedalea: induced development and effects on competitors. Mar. Ecol. Prog. Ser. 282, 161–171. https://doi.org/10.3354/meps282161 (2004).
ADS  Article  Google Scholar 

32.
Bak, R. P. M., Termaat, R. M. & Dekker, R. Complexity of coral interactions: influence of time, location of interaction and epifauna. Mar. Biol. 69, 215–222. https://doi.org/10.1007/BF00396901 (1982).
Article  Google Scholar 

33.
Lapid, E. D. & Chadwick, N. E. Long-term effects of competition on coral growth and sweeper tentacle development. Mar. Ecol. Prog. Ser. 313, 115–123. https://doi.org/10.3354/meps313115 (2006).
ADS  Article  Google Scholar 

34.
Millar, K. J. The Platygyra species complex: implications for coral taxonomy and evolution. Dissertation, James Cook University of North Queensland (1994).

35.
Dai, C. F. Interspecific competition in Taiwanese corals with special reference to interactions between alcyonaceans and scleractinians. Mar. Ecol. Prog. Ser. 60, 291–297 (1990).
ADS  Article  Google Scholar 

36.
Forsman, Z. H., Page, C. A., Toonen, R. J. & Vaughan, D. Growing coral larger and faster: micro-colony-fusion as a strategy for accelerating coral cover. PeerJ 3, e1313. https://doi.org/10.7717/peerj.1313 (2015).
CAS  Article  PubMed  PubMed Central  Google Scholar 

37.
Colinvaux, P. A. Introduction to Ecology (Wiley, New York, 1973).
Google Scholar 

38.
Lang, J. C. Interspecific aggression by scleractinian corals. II. Why the race is not always to the swift. Bull. Mar. Sci. 23, 260–279 (1973).
Google Scholar 

39.
Rinkevich, B. & Loya, Y. Oriented translocation of energy in grafted reef corals. Coral Reefs 1, 243–247. https://doi.org/10.1007/BF00304422 (1983).
ADS  Article  Google Scholar 

40.
Chornesky, E. A. The ties that bind: inter-clonal cooperation may help a fragile coral dominate shallow high-energy reefs. Mar. Biol. 109, 41–51. https://doi.org/10.1007/BF01320230 (1991).
Article  Google Scholar 

41.
Rejmanek, M. Intraspecific aggregation and species coexistence. Trends Ecol. Evol. 17, 209–210 (2002).
Article  Google Scholar 

42.
Karlson, R. H., Cornell, H. V. & Hughes, T. P. Aggregation influences coral species richness at multiple spatial scales. Ecology 88, 170–177. https://doi.org/10.1890/0012-9658(2007)88[170:AICSRA]2.0.CO;2 (2007).
Article  PubMed  Google Scholar 

43.
Idjadi, J. A. & Karlson, R. H. Spatial arrangement of competitors influences coexistence of reef-building corals. Ecology 88, 2449–2454. https://doi.org/10.1890/06-2031.1 (2007).
Article  PubMed  Google Scholar 

44.
Edmunds, P. J. & Davies, P. S. An energy budget for Porites porites (Scleractinia). Mar. Biol. 92, 339–347. https://doi.org/10.1007/BF00392674 (1986).
Article  Google Scholar 

45.
Vollmer, S. V. & Edmunds, P. J. Allometric scaling in small colonies of the scleractinian coral Siderastrea siderea (Ellis and Solander). Biol. Bull. 199, 21–28. https://doi.org/10.2307/1542703 (2000).
CAS  Article  PubMed  Google Scholar 

46.
Buss, L. W. Bryozoan overgrowth interactions—the interdependence of competition for space and food. Nature 281, 475–477. https://doi.org/10.1038/281475a0 (1979).
ADS  Article  Google Scholar 

47.
Thongtham, N. & Chansang, H. Transplantation of Porites lutea to rehabilitate degraded coral reef at Maiton Island, Phuket, Thailand. in Proceedings of the 11th International Coral Reef Symposium, 1271–1274 (2009).

48.
dela Cruz, D. W., Rinkevich, B., Gomez, E. D. & Yap, H. T. Assessing an abridged nursery phase for slow growing corals used in coral restoration. Ecol. Eng. 84, 408–415. https://doi.org/10.1016/j.ecoleng.2015.09.042 (2015).
Article  Google Scholar 

49.
Forrester, G. E., Ferguson, M. A., O’Connell-Rodwell, C. E. & Jarecki, L. L. Long-term survival and colony growth of Acropora palmata fragments transplanted by volunteers for restoration. Aquat. Conserv. 24, 81–91. https://doi.org/10.1002/aqc.2374 (2014).
Article  Google Scholar 

50.
Edwards, A. J. & Clark, S. Coral transplantation: a useful management tool or misguided meddling?. Mar. Pollut. Bull. 37, 474–487. https://doi.org/10.1016/S0025-326X(99)00145-9 (1999).
Article  Google Scholar 

51.
Harrison, P. L. & Wallace, C. C. Reproduction, dispersal and recruitment of scleractinian corals. In Coral Reefs. Ecosystems of the World (ed. Dubinski, Z.) 133–206 (Elsevier, Amsterdam, 1990).
Google Scholar 

52.
Koh, E. G. L. & Sweatman, H. Chemical warfare among scleractinians: bioactive natural products from Tubastrea faulkneri Wells kill larvae of potential competitors. J. Exp. Mar. Biol. Ecol. 251, 141–160. https://doi.org/10.1016/S0022-0981(00)00222-7 (2000).
CAS  Article  PubMed  Google Scholar 

53.
Van Veghel, M. L. J., Cleary, D. F. R. & Bak, R. P. M. Interspecific interactions and the competitive ability of the polymorphic reef-building coral Montastraea annularis. Bull. Mar. Sci. 58, 792–803 (1996).
Google Scholar 

54.
Edwards, A. J. et al. Evaluating costs of restoration. In Reef Restoration Manual (ed. Edwards, A. J.) 113–128 (Coral Reef Targeted Research & Capacity Building for Management Program, St Lucia, 2010).
Google Scholar 

55.
Huang, D. W., Tun, K. P. P., Chou, L. M. & Todd, P. A. An inventory of zooxanthellate scleractinian corals in Singapore, including 33 new records. Raffles B Zool. 22, 69–80 (2009).
CAS  Google Scholar 

56.
Forsman, Z. H., Rinkevich, B. & Hubter, C. L. Investigating fragment size for culturing reef-building corals (Porites lobata and P. compressa) in ex situ nurseries. Aquaculture 261, 89–97. https://doi.org/10.1016/j.aquaculture.2006.06.040 (2006).
Article  Google Scholar  More