More stories

  • in

    Climate change alters impacts of extreme climate events on a tropical perennial tree crop

    Using a robust recent dataset, our analyses show that cocoa production is significantly affected by the maximum magnitude of ENSO phase during the current and previous purchase years (Fig. 2). The instantaneous effect is negative, followed by delayed positive effects in the two following years and negative in the third following year, combining to give a picture of multi-year fluctuations in cocoa production as a result of El Niño/La Niña events. Using a 70-year dataset, we show significant changes in these instantaneous and delayed ENSO-production relationships between recent and past time periods (Fig. 3). Using ERA5 data for the cocoa production area of Ghana, summarised at the same temporal resolution as the production data, we demonstrate significant relationships between ENSO phase and climate, with significant changes in mean climate and in ENSO-climate relationships (Fig. 4) between recent and past time periods. This agrees with prior work suggesting that ENSO may impact West Africa5,15, despite no current evidence of teleconnections between ENSO phase and West African climate17.Our 70-year production dataset represents a temporal extent unmatched by other research, however was aggregated to fewer replicates than the 21-year analysis (6 regions vs 68 districts). While this may represent reduced power, results from the overlapping time period of the two datasets strongly agree. The computation of yield, a more comparable metric between different-sized areas than total production, was not possible because data on area under production (AUP) were not available. However, the detrending process employed successfully eliminated variation between districts or regions (of which AUP is likely a substantial component) and long-term technological trends that would otherwise confound our ability to isolate the ENSO signal (Supplementary results).Perennial crops have multi-year growing patterns, with allocation of resources to growth, development and reproduction driven by climate in ways that are not fully understood29. ENSO generally peaks between October and December, also the busiest cocoa purchase period: thus we observe a relatively instantaneous apparent effect of ENSO phase on cocoa production. This reduction in cocoa production under El Niño inis consistent with results from farm monitoring8 and large-scale farm surveys30 evidencing production declines in from other regions (where teleconnections are understood), and with analyses of production data from West Africa31. During the main cocoa purchase period, coinciding with the minor wet and major dry seasons, we observe increases in water deficit during El Niño, leading to drought stress conditions. In small-scale cocoa studies, drought stress is correlated with reduction in pod production and increased tree mortality8,32, and in similar studies of other tree crops drought is directly linked to reduction in fruit or nut production33, although in all cases the mechanisms are unclear. Drought may generally create unfavourable conditions for growth and reproduction through reduced availability of water for vital processes, or more specifically by promoting disease incidence and pod rot8, increasing the chance of fire, increasing competition for soil moisture32, and/or reducing pollinator populations34. Alternatively, cocoa may respond to reduced water availability by reallocation of resources away from energetically expensive reproduction: rainfall exclusion experiments suggest that in the medium term, while bean production drops, vegetative growth is not significantly reduced during drought32.The significant increases in mean temperature and average drought stress we observed in some seasons over time is such that the climate experienced during El Niño events in recent decades represent novel extreme conditions for Ghana’s cocoa agriculture. This causes significant changes in the responses of cocoa production to ENSO phase over the same time period. One explanation for this may be that the warm, dry El Niño conditions in Ghana in the past were within the environmental tolerance of cocoa, leading to allocation of resources to reproduction in response to drought, increasing cocoa bean production and resulting in less severe instantaneous and delayed responses to ENSO phase (Fig. 3a–d) However, in recent decades this level or greater drought stress has become the norm (Fig. 4i–l), with El Niño conditions apparently triggering a different response mode, allocating resources away from reproduction in the short term and creating oscillating resource allocation over the following years.However, understanding the delayed responses of cocoa is challenging, especially as these represent a novel finding. There is little research that explores multi-annual physiological or ecological responses of cocoa to drought, and the explanation is likely to be a combination of both residual/delayed climatic responses to ENSO phase, and of life history strategies. The observed increase in production during the two years following El Niño may be explained by post-drought reallocation of resources to reproduction as remediation for lost reproductive output in the instantaneous response, or a shift to a ‘faster’ strategy by allocating resources to reproduction over the longer term, becoming evident in the data in subsequent years. Alternatively, this may be explained by favourable climatic conditions occurring during an El Niño event that impact the following years’ crop. March and April is a crucial time for cocoa pod development in Ghana and in recent years El Niño appears to bring greater rainfall during these months. Given the 6–9 months development of cocoa beans, the effects of this increased rainfall and reduced water deficit on cocoa production will be seen in the delayed response. We see evidence of this in the climate-change driven reversal of March–April rainfall patterns: while in the past El Niño has consistently resulted in drought stress, this reversal provides a respite from drought, buffering trees from reduced rainfall during the major wet season and giving sufficient resources for improved production in the following year.The robustness of our results provide evidence that may aid development of resilience strategies for ENSO-driven cocoa production variation in Ghana, but we may also consider whether these results can be generalised to the production of cocoa and/or perennial tree crops globally. The climatic impact of ENSO observed in Ghana is broadly consistent with many regions of the tropics2, the instantaneous cocoa production responses to El Niño are consistent with findings in these regions, and so we may expect these regions to see a similar pattern of multi-annual cocoa production variation in response to ENSO phase. However, there is considerable variation in ENSO responses among and within other perennial tree crops in regions where climatic responses to ENSO are similar to Ghana. Oil palm yields have been negatively associated with ENSO phase in Malaysia9, as have olive yields in Morocco (delayed by a year)33. Conversely, apple yields have been positively associated with ENSO phase in China10, as have coffee yields in Brazil35; however, no effect at all is seen in coffee in India over a 35-year time series7. Most of these analyses considered only a single ENSO phase (usually El Niño), and most considered only instantaneous impacts. However, it is clear that most of these crops do respond to ENSO, and given the shared biology it is reasonable to assume that delayed effects of ENSO phase are likely and should be considered to understand the full picture of ENSO impacts on perennial tree crops.The larger body of research into ENSO impacts on annual crops includes many studies using long time series, reporting high heterogeneity in space and among crops11,36,37. However, there appears to be little examination of changes in the direction and magnitude of ENSO responses over time; thus our findings are timely and signal that further research is needed to examine how changing climates may force novel extreme climatic conditions and shift response patterns to ENSO phase. Given that perennial tree crops are generally cash crops, and the utility of these crops to farmers are to a greater or lesser extent mediated by market forces, there is a need for improved forecasting of yield in response to changing climate and ENSO patterns to withstand production fluctuations. The low perishability of many perennial tree crops means that with accurate forecasting, supply may be managed or even exploited to ensure consistency of income both for farmers and those whose livelihoods depend on related food manufacturing industries.Our approach to understanding the responses of a perennial tree crop to ENSO phase and anthropogenic climate change exploited existing global, national and subnational datasets for climate and production with appropriate spatial and temporal resolution. We use freely available geographic and climate data, and employ highly replicable methods: a simple pipeline of climate data aggregation and summary computation, coupled with standard detrending and straightforward analytical methods with a relatively small computational requirement. This “big data” approach to agriculture-climate research demonstrates a relatively straightforward framework for understanding responses of agricultural productivity to climate and identifying temporal changes in these relationships. While small-scale studies examine the mechanisms of climate impacts through the interacting effects of agricultural practices, abiotic conditions, disease incidence and multi-trophic interactions, large-scale studies across regions and over time scales encompassing many ENSO oscillations are required to understand the global picture of perennial tree crop production security. Combined with local context-specific studies on governance arrangements16, such approaches could be crucial for reducing future vulnerability of these industries to increasing volatility under anthropogenic climate change. The main barrier to this research is the availability of production data from state or commercial entities. More

  • in

    Intensive grassland management disrupts below-ground multi-trophic resource transfer in response to drought

    Bardgett, R. D. et al. Combatting global grassland degradation. Nat. Rev. Earth Environ. 2, 720–735 (2021)Reichstein, M. et al. Climate extremes and the carbon cycle. Nature 500, 287–295 (2013).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Seneviratne, S. I. et al. Weather and climate extreme events in a changing climate. In Climate change 2021: the physical science basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change (Cambridge University Press, 2021).Pretty, J. et al. Global assessment of agricultural system redesign for sustainable intensification. Nat. Sustain 1, 441–446 (2018).
    Google Scholar 
    Allan, E. et al. Land use intensification alters ecosystem multifunctionality via loss of biodiversity and changes to functional composition. Ecol. Lett. 18, 834–843 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    Bardgett, R. D. & Cook, R. Functional aspects of soil animal diversity in agricultural grasslands. Appl. Soil Ecol. 10, 263–276 (1998).
    Google Scholar 
    Postma-Blaauw, M. B., de Goede, R. G. M., Bloem, J., Faber, J. H. & Brussaard, L. Soil biota community structure and abundance under agricultural intensification and extensification. Ecology 91, 460–473 (2010).PubMed 

    Google Scholar 
    Vályi, K., Rillig, M. C. & Hempel, S. Land-use intensity and host plant identity interactively shape communities of arbuscular mycorrhizal fungi in roots of grassland plants. N. Phytologist 205, 1577–1586 (2015).
    Google Scholar 
    de Vries, F. T., Hoffland, E., van Eekeren, N., Brussaard, L. & Bloem, J. Fungal/bacterial ratios in grasslands with contrasting nitrogen management. Soil Biol. Biochem. 38, 2092–2103 (2006).
    Google Scholar 
    de Vries, F. T. et al. Extensive Management Promotes Plant and Microbial Nitrogen Retention in Temperate Grassland. PLoS ONE 7, e51201 (2012).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    de Vries, F. T., van Groenigen, J. W., Hoffland, E. & Bloem, J. Nitrogen losses from two grassland soils with different fungal biomass. Soil Biol. Biochem. 43, 997–1005 (2011).
    Google Scholar 
    Malik, A. A. et al. Soil fungal: bacterial ratios are linked to altered carbon cycling. Front. Microbiol. 7, 1247 (2016).Bardgett, R. D., Streeter, T. C. & Bol, R. Soil Microbes Compete Effectively with Plants for Organic-Nitrogen Inputs to Temperate Grasslands. Ecology 84, 1277–1287 (2003).
    Google Scholar 
    Bardgett, R. D. & McAlister, E. The measurement of soil fungal:bacterial biomass ratios as an indicator of ecosystem self-regulation in temperate meadow grasslands. Biol. Fertil. Soils 29, 282–290 (1999).
    Google Scholar 
    Gordon, H., Haygarth, P. M. & Bardgett, R. D. Drying and rewetting effects on soil microbial community composition and nutrient leaching. Soil Biol. Biochem. 40, 302–311 (2008).CAS 

    Google Scholar 
    Duffy, J. E. et al. The functional role of biodiversity in ecosystems: incorporating trophic complexity. Ecol. Lett. 10, 522–538 (2007).PubMed 

    Google Scholar 
    Wang, S. & Brose, U. Biodiversity and ecosystem functioning in food webs: the vertical diversity hypothesis. Ecol. Lett. 21, 9–20 (2018).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Ruf, A., Kuzyakov, Y. & Lopatovskaya, O. Carbon fluxes in soil food webs of increasing complexity revealed by C-14 labelling and C-13 natural abundance. Soil Biol. Biochem. 38, 2390–2400 (2006).CAS 

    Google Scholar 
    Pollierer, M. M., Langel, R., Koerner, C., Maraun, M. & Scheu, S. The underestimated importance of belowground carbon input for forest soil animal food webs. Ecol. Lett. 10, 729–736 (2007).PubMed 

    Google Scholar 
    Eissfeller, V. et al. Incorporation of plant carbon and microbial nitrogen into the rhizosphere food web of beech and ash. Soil Biol. Biochem. 62, 76–81 (2013).CAS 

    Google Scholar 
    Gilbert, K. J. et al. Exploring carbon flow through the root channel in a temperate forest soil food web. Soil Biol. Biochem. 76, 45–52 (2014).CAS 

    Google Scholar 
    Goncharov, A. A., Tsurikov, S. M., Potapov, A. M. & Tiunov, A. V. Short-term incorporation of freshly fixed plant carbon into the soil animal food web: field study in a spruce forest. Ecol. Res. 31, 923–933 (2016).CAS 

    Google Scholar 
    Chomel, M. et al. Drought decreases incorporation of recent plant photosynthate into soil food webs regardless of their trophic complexity. Glob. Change Biol. 25, 3549–3561 (2019).ADS 

    Google Scholar 
    Moore, J. C., de Ruiter, P. C. & Hunt, H. W. Influence of productivity on the stability of real and model ecosystems. Science 261, 906–908 (1993).ADS 
    CAS 
    PubMed 
    MATH 

    Google Scholar 
    de Ruiter, P. C., Neutel, A.-M. & Moore, J. C. Energetics, Patterns of Interaction Strengths, and Stability in Real Ecosystems. Science 269, 1257–1260 (1995).ADS 
    PubMed 

    Google Scholar 
    Rooney, N., McCann, K., Gellner, G. & Moore, J. C. Structural asymmetry and the stability of diverse food webs. Nature 442, 265–269 (2006).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Rooney, N. & McCann, K. S. Integrating food web diversity, structure and stability. Trends Ecol. Evolution 27, 40–46 (2012).
    Google Scholar 
    de Vries, F. T. et al. Land use alters the resistance and resilience of soil food webs to drought. Nat. Clim. Change 2, 276 (2012).ADS 

    Google Scholar 
    Ingrisch, J. et al. Land Use Alters the Drought Responses of Productivity and CO2 Fluxes in Mountain Grassland. Ecosystems 21, 689–703 (2018).PubMed 

    Google Scholar 
    Karlowsky, S. et al. Land use in mountain grasslands alters drought response and recovery of carbon allocation and plant‐microbial interactions. J. Ecol. 106, 1230–1243 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    Vilonen, L., Ross, M. & Smith, M. D. What happens after drought ends: synthesizing terms and definitions. N. Phytologist 235, 420–431 (2022).
    Google Scholar 
    Ingrisch, J., Karlowsky, S., Hasibeder, R., Gleixner, G. & Bahn, M. Drought and recovery effects on belowground respiration dynamics and the partitioning of recent carbon in managed and abandoned grassland. Glob. Change Biol. 26, 4366–4378 (2020).ADS 

    Google Scholar 
    Ward, S. E. et al. Legacy effects of grassland management on soil carbon to depth. Glob. Change Biol. 22, 2929–2938 (2016).ADS 

    Google Scholar 
    Henry, C. et al. A stomatal safety-efficiency trade-off constrains responses to leaf dehydration. Nat. Commun. 10, 3398 (2019).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Baptist, F. et al. 13C and 15N allocations of two alpine species from early and late snowmelt locations reflect their different growth strategies. J. Exp. Bot. 60, 2725–2735 (2009).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Bergmann, J. et al. The fungal collaboration gradient dominates the root economics space in plants. Sci. Adv. 6, eaba3756 (2020).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Williams, A. et al. Root functional traits explain root exudation rate and composition across a range of grassland species. J. Ecol. 110, 21–33 (2022).
    Google Scholar 
    Deyn, G. B. D., Quirk, H., Oakley, S., Ostle, N. J. & Bartgett, R. D. Rapid transfer of photosynthetic carbon through the plant-soil system in differently managed species-rich grasslands. Biogeosciences 8, 1131–1139 (2011).Pausch, J. et al. Small but active – pool size does not matter for carbon incorporation in below‐ground food webs.Functional Ecol. 30, 479–489 (2016).
    Google Scholar 
    Morriën, E. et al. Soil networks become more connected and take up more carbon as nature restoration progresses. Nat. Commun. 8, 14349 (2017).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Li, Z. et al. The flux of root-derived carbon via fungi and bacteria into soil microarthropods (Collembola) differs markedly between cropping systems. Soil Biol. Biochem. 160, 108336 (2021).CAS 

    Google Scholar 
    Joergensen, R. Ergosterol and microbial biomass in the rhizosphere of grassland soils. Soil Biol. Biogeochemistry 32, 647–652 (2000).CAS 

    Google Scholar 
    Staddon, P. L., Ramsey, C. B., Ostle, N., Ineson, P. & Fitter, A. H. Rapid Turnover of Hyphae of Mycorrhizal Fungi Determined by AMS Microanalysis of 14C. Science 300, 1138–1140 (2003).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Johnson, D., Leake, J. R., Ostle, N., Ineson, P. & Read, D. J. In situ 13CO2 pulse-labelling of upland grassland demonstrates a rapid pathway of carbon flux from arbuscular mycorrhizal mycelia to the soil. N. Phytologist 153, 327–334 (2002).CAS 

    Google Scholar 
    Johnson, D., Leake, J. R. & Read, D. J. Transfer of recent photosynthate into mycorrhizal mycelium of an upland grassland: short-term respiratory losses and accumulation of C-14. Soil Biol. Biochem. 34, 1521–1524 (2002).CAS 

    Google Scholar 
    Schimel, J., Balser, T. C. & Wallenstein, M. Microbial Stress-Response Physiology and Its Implications for Ecosystem Function. Ecology 88, 1386–1394 (2007).PubMed 

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

    Google Scholar 
    Manzoni, S., Schimel, J. P. & Porporato, A. Responses of soil microbial communities to water stress: results from a meta-analysis. Ecology 93, 930–938 (2012).PubMed 

    Google Scholar 
    Holden, S. R. & Treseder, K. K. A meta-analysis of soil microbial biomass responses to forest disturbances. Front Microbiol 4, 163 (2013).PubMed 
    PubMed Central 

    Google Scholar 
    Guhr, A., Borken, W., Spohn, M. & Matzner, E. Redistribution of soil water by a saprotrophic fungus enhances carbon mineralization. PNAS 112, 14647–14651 (2015).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    de Vries, F. T. et al. Soil bacterial networks are less stable under drought than fungal networks. Nat. Commun. 9, 3033 (2018).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Allen, M. F. Mycorrhizal Fungi: Highways for Water and Nutrients in Arid Soils. Vadose Zone J. 6, 291–297 (2007).
    Google Scholar 
    Kakouridis, A. et al. Routes to roots: direct evidence of water transport by arbuscular mycorrhizal fungi to host plants. bioRxiv https://doi.org/10.1101/2020.09.21.305409 (2020).Leake, J. R., Ostle, N. J., Rangel-Castro, J. I. & Johnson, D. Carbon fluxes from plants through soil organisms determined by field 13CO2 pulse-labelling in an upland grassland. Appl. Soil Ecol. 33, 152–175 (2006).
    Google Scholar 
    Maaß, S., Migliorini, M., Rillig, M. C. & Caruso, T. Disturbance, neutral theory, and patterns of beta diversity in soil communities. Ecol. Evolution 4, 4766–4774 (2014).
    Google Scholar 
    Barnard, R. L., Osborne, C. A. & Firestone, M. K. Changing precipitation pattern alters soil microbial community response to wet-up under a Mediterranean-type climate. ISME J. 9, 946–957 (2015).CAS 
    PubMed 

    Google Scholar 
    Lennon, J. T. & Jones, S. E. Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat. Rev. Microbiol 9, 119–130 (2011).CAS 
    PubMed 

    Google Scholar 
    Meisner, A., Bååth, E. & Rousk, J. Microbial growth responses upon rewetting soil dried for four days or one year. Soil Biol. Biochem. 66, 188–192 (2013).CAS 

    Google Scholar 
    Meisner, A., Rousk, J. & Bååth, E. Prolonged drought changes the bacterial growth response to rewetting. Soil Biol. Biochem. 88, 314–322 (2015).CAS 

    Google Scholar 
    Blazewicz, S. J., Schwartz, E. & Firestone, M. K. Growth and death of bacteria and fungi underlie rainfall-induced carbon dioxide pulses from seasonally dried soil. Ecology 95, 1162–1172 (2014).PubMed 

    Google Scholar 
    Butterbach-Bahl, K., Baggs, E. M., Dannenmann, M., Kiese, R. & Zechmeister-Boltenstern, S. Nitrous oxide emissions from soils: how well do we understand the processes and their controls? Philos. Trans. R. Soc. B: Biol. Sci. 368, 20130122 (2013).
    Google Scholar 
    Baggs, E. M., Rees, R. M., Smith, K. A. & Vinten, A. J. A. Nitrous oxide emission from soils after incorporating crop residues. Soil Use & Manag. 16, 82–87 (2000).
    Google Scholar 
    Le Roux, X., Bardy, M., Loiseau, P. & Louault, F. Stimulation of soil nitrification and denitrification by grazing in grasslands: do changes in plant species composition matter? Oecologia 137, 417–425 (2003).ADS 
    PubMed 

    Google Scholar 
    Morley, N. & Baggs, E. M. Carbon and oxygen controls on N2O and N2 production during nitrate reduction. Soil Biol. Biochem. 42, 1864–1871 (2010).CAS 

    Google Scholar 
    Davidson, E. A. & Kanter, D. Inventories and scenarios of nitrous oxide emissions. Environ. Res. Lett. 9, 105012 (2014).ADS 

    Google Scholar 
    Bateman, E. J. & Baggs, E. M. Contributions of nitrification and denitrification to N2O emissions from soils at different water-filled pore space. Biol. Fertil. Soils 41, 379–388 (2005).CAS 

    Google Scholar 
    Lehmann, J., Bossio, D. A., Kögel-Knabner, I. & Rillig, M. C. The concept and future prospects of soil health. Nat. Rev. Earth Environ. 1, 544–553 (2020).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Knapp, A. K. et al. Pushing precipitation to the extremes in distributed experiments: recommendations for simulating wet and dry years. Glob. Change Biol. 23, 1774–1782 (2017).ADS 

    Google Scholar 
    Cole, A. J. et al. Grassland biodiversity restoration increases resistance of carbon fluxes to drought. J. Appl. Ecol. 56, 1806–1816 (2019).CAS 

    Google Scholar 
    Fuchslueger, L., Bahn, M., Fritz, K., Hasibeder, R. & Richter, A. Experimental drought reduces the transfer of recently fixed plant carbon to soil microbes and alters the bacterial community composition in a mountain meadow. N. Phytologist 201, 916–927 (2014).CAS 

    Google Scholar 
    Buyer, J. S. & Sasser, M. High throughput phospholipid fatty acid analysis of soils. Appl. Soil Ecol. 61, 127–130 (2012).
    Google Scholar 
    Frostegård, Å., Bååth, E. & Tunlio, A. Shifts in the structure of soil microbial communities in limed forests as revealed by phospholipid fatty acid analysis. Soil Biol. Biochem. 25, 723–730 (1993).
    Google Scholar 
    Olsson, P. A., Thingstrup, I., Jakobsen, I. & Bååth, E. Estimation of the biomass of arbuscular mycorrhizal fungi in a linseed field. Soil Biol. Biochem. 31, 1879–1887 (1999).CAS 

    Google Scholar 
    Hopkin, S. P. A key to the Collembola (springtails) of Britain and Ireland (FSC, 2007).Krantz, G. W. & Walter, D. E. A manual of acarology (Texas Tech Universty Press, 2009).Caruso, T. & Migliorini, M. Euclidean geometry explains why lengths allow precise body mass estimates in terrestrial invertebrates: The case of oribatid mites. J. Theor. Biol. 256, 436–440 (2009).ADS 
    MathSciNet 
    CAS 
    PubMed 
    MATH 

    Google Scholar 
    Ganihar, S. R. Biomass estimates of terrestrial arthropods based on body length. J. Biosci. 22, 219–224 (1997).
    Google Scholar 
    Johnson, D., Vachon, J., Britton, A. J. & Helliwell, R. C. Drought alters carbon fluxes in alpine snowbed ecosystems through contrasting impacts on graminoids and forbs. N. Phytologist 190, 740–749 (2011).CAS 

    Google Scholar 
    Legendre, P. & Gallagher, E. D. Ecologically meaningful transformations for ordination of species data. Oecologia 129, 271–280 (2001).ADS 
    PubMed 

    Google Scholar 
    Anderson, M. J. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 26, 32–46 (2001).
    Google Scholar 
    Anderson, M. J. Distance-Based Tests for Homogeneity of Multivariate Dispersions. Biometrics 62, 245–253 (2006).MathSciNet 
    PubMed 
    MATH 

    Google Scholar 
    Zuur, A., Ieno, E., Walker, N., Saveliev, A. & Smith, G. Mixed effects models and extensions in ecology with R. (Springer, 2009). More

  • in

    Modelling the Mediterranean Sea ecosystem at high spatial resolution to inform the ecosystem-based management in the region

    Barbier, E. B. Marine ecosystem services. Curr. Biol. 27, R507–R510 (2017).CAS 
    PubMed 

    Google Scholar 
    Liquete, C., Piroddi, C., Macías, D., Druon, J.-N. & Zulian, G. Ecosystem services sustainability in the Mediterranean Sea: Assessment of status and trends using multiple modelling approaches. Sci. Rep. 6, 34162 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Halpern, B. S. et al. Recent pace of change in human impact on the world’s ocean. Sci. Rep. 9, 1–8 (2019).CAS 

    Google Scholar 
    Duarte, C. M. et al. Rebuilding marine life. Nature 580, 39–51 (2020).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Long, R. D., Charles, A. & Stephenson, R. L. Key principles of marine ecosystem-based management. Mar. Policy 57, 53–60 (2015).
    Google Scholar 
    Link, J. S. & Browman, H. I. Operationalizing and implementing ecosystem-based management. ICES J. Mar. Sci. 74, 379–381 (2017).
    Google Scholar 
    EC. A Farm to Fork Strategy for a Fair, Healthy and Environmentally-Friendly Food System. Brussels: European Commission. (2020).EC. Communication from the Commission to the European Parliament, the Council, the European Economic and Social Committee and the Committee of the Regions, “Pathway to a healthy planet for all” with the sub-title “EU action Plan: ’Towards zero pollution for air, water and soil, COM (2021) 400. (2021).EC. The European Green Deal. Communication from the Commission to the European Parliament, the European Council, the European Economic and Social Committee and the Committee of the Regions, COM (2019) 640. (2019).Alexander, K. & Haward, M. The human side of marine ecosystem-based management (EBM): ‘Sectoral interplay’ as a challenge to implementing EBM. Mar. Policy 101, 33–38 (2019).
    Google Scholar 
    EC. The EU Blue Economy Report 2021. (2021).Ostlaender, N. et al. Modelling Inventory and Knowledge Man-agement System of the European Commission (MIDAS) (Publications Office of the European Union, 2019).
    Google Scholar 
    Friedland, R. et al. Effects of nutrient management scenarios on marine eutrophication indicators: A Pan-European, multi-model assessment in support of the Marine Strategy Framework Directive. Front. Mar. Sci. 8, 596126 (2021).
    Google Scholar 
    Piroddi, C. et al. Effects of nutrient management scenarios on marine food webs: A Pan-European Assessment in support of the Marine Strategy Framework Directive. Front. Mar. Sci. 8, 179 (2021).
    Google Scholar 
    Corrales, X. et al. Multi-zone marine protected areas: Assessment of ecosystem and fisheries benefits using multiple ecosystem models. Ocean Coast. Manag. 193, 105232 (2020).
    Google Scholar 
    Bentley, J. W. et al. Refining fisheries advice with stock-specific ecosystem information. Front. Mar. Sci. 8, 602072 (2021).
    Google Scholar 
    Steenbeek, J. et al. Making spatial-temporal marine ecosystem modelling better—A perspective. Environ. Model. Softw. 145, 105209 (2021).PubMed 
    PubMed Central 

    Google Scholar 
    Heymans, J. J. et al. The ocean decade: A true ecosystem modelling challenge. Front. Mar. Sci. 7, 554573 (2020).
    Google Scholar 
    Hernvann, P.-Y. et al. The Celtic sea through time and space: Ecosystem modeling to unravel fishing and climate change impacts on food-web structure and dynamics. Front. Mar. Sci. 7, 1018 (2020).
    Google Scholar 
    Christensen, V. & Walters, C. J. Ecopath with Ecosim: Methods, capabilities and limitations. Ecol. Model. 172, 109–139 (2004).
    Google Scholar 
    Steenbeek, J. et al. Bridging the gap between ecosystem modeling tools and geographic information systems: Driving a food web model with external spatial–temporal data. Ecol. Model. 263, 139–151 (2013).
    Google Scholar 
    Christensen, V. et al. Representing variable habitat quality in a spatial food web model. Ecosystems 17, 1397–1412 (2014).CAS 

    Google Scholar 
    de Mutsert, K., Lewis, K., Milroy, S., Buszowski, J. & Steenbeek, J. Using ecosystem modeling to evaluate trade-offs in coastal management: Effects of large-scale river diversions on fish and fisheries. Ecol. Model. 360, 14–26 (2017).
    Google Scholar 
    Serpetti, N. et al. Modelling small scale impacts of Multi-Purpose Platforms: An ecosystem approach. Front. Mar. Sci. 8, 778 (2021).
    Google Scholar 
    DFO. Technical review of Roberts Bank Terminal 2 environmental assessment: section 10.3—assessing ecosystem productivity. DFO Can. Sci. Advis. Sec. Sci. Resp. 2016/050 (2016).Coll, M., Pennino, M. G., Steenbeek, J., Solé, J. & Bellido, J. M. Predicting marine species distributions: Complementarity of food-web and Bayesian hierarchical modelling approaches. Ecol. Model. 405, 86–101 (2019).
    Google Scholar 
    Coll, M. et al. The biodiversity of the Mediterranean Sea: Estimates, patterns, and threats. PLoS One 5, e11842 (2010).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Coll, M. et al. The Mediterranean Sea under siege: Spatial overlap between marine biodiversity, cumulative threats and marine reserves. Glob. Ecol. Biogeogr. 21, 465–480 (2012).
    Google Scholar 
    Micheli, F. et al. Cumulative human impacts on mediterranean and black sea marine ecosystems: Assessing current pressures and opportunities. PLoS One 8, e79889 (2013).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Piroddi, C., Colloca, F. & Tsikliras, A. C. The living marine resources in the Mediterranean Sea large marine ecosystem. Environ. Dev. 36, 100555 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    Barale, V. & Gade, M. Remote Sensing of the European Seas. (Springer, 2008).Siokou-Frangou, I. et al. Plankton in the open Mediterranean Sea: A review. Biogeosciences 7, 1543–1586 (2010).ADS 

    Google Scholar 
    Spalding, M. D. et al. Marine ecoregions of the world: A bioregionalization of coastal and shelf areas. Bioscience 57, 573–583 (2007).
    Google Scholar 
    Bianchi, C. N. et al. In Life in the Mediterranean Sea: A Look at Habitat Changes, vol. 1 55 (2012).Danovaro, R. et al. Deep-sea biodiversity in the Mediterranean Sea: The known, the unknown, and the unknowable. PLoS One 5, e11832 (2010).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Moullec, F. et al. Capturing the big picture of Mediterranean marine biodiversity with an end-to-end model of climate and fishing impacts. Prog. Oceanogr. 178, 102179 (2019).
    Google Scholar 
    Macias, D., Garcia-Gorriz, E., Piroddi, C. & Stips, A. Biogeochemical control of marine productivity in the Mediterranean Sea during the last 50 years. Glob. Biogeochem. Cycles 28, 897–907 (2014).ADS 
    CAS 

    Google Scholar 
    Piroddi, C. et al. Historical changes of the Mediterranean Sea ecosystem: Modelling the role and impact of primary productivity and fisheries changes over time. Sci. Rep. 7, 44491 (2017).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Lotze, H. K. et al. Depletion, degradation, and recovery potential of estuaries and coastal seas. Science 312, 1806–1809 (2006).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Lotze, H. K., Coll, M. & Dunne, J. A. Historical changes in marine resources, food-web structure and ecosystem functioning in the Adriatic Sea, Mediterranean. Ecosystems 14, 198–222 (2011).
    Google Scholar 
    Macias, D., Huertas, I. E., Garcia-Gorriz, E. & Stips, A. Non-Redfieldian dynamics driven by phytoplankton phosphate frugality explain nutrient and chlorophyll patterns in model simulations for the Mediterranean Sea. Prog. Oceanogr. 173, 37–50 (2019).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Spedicato, M. T. et al. The MEDITS trawl survey specifications in an ecosystem approach to fishery management. Sci. Mar. 83, 9–20 (2019).
    Google Scholar 
    Corrales, X. et al. Hindcasting the dynamics of an Eastern Mediterranean marine ecosystem under the impacts of multiple stressors. Mar. Ecol. Prog. Ser. 580, 17–36 (2017).ADS 

    Google Scholar 
    FAO. The State of the Mediterranean and Black Sea fisheries (General Fisheries Commission for the Mediterranean (GFCM), 2020).Ferrà, C. et al. Mapping change in bottom trawling activity in the Mediterranean Sea through AIS data. Mar. Policy 94, 275–281 (2018).
    Google Scholar 
    Russo, T. et al. Trends in effort and yield of trawl fisheries: A case study from the Mediterranean Sea. Front. Mar. Sci. 6, 153 (2019).ADS 

    Google Scholar 
    Ramírez, F., Coll, M., Navarro, J., Bustamante, J. & Green, A. J. Spatial congruence between multiple stressors in the Mediterranean Sea may reduce its resilience to climate impacts. Sci. Rep. 8, 1–8 (2018).
    Google Scholar 
    Coll, M., Steenbeek, J., Ben Rais Lasram, F., Mouillot, D. & Cury, P. ‘Low-hanging fruit’ for conservation of marine vertebrate species at risk in the Mediterranean Sea. Glob. Ecol. Biogeogr. 24, 226–239 (2015).
    Google Scholar 
    Ruiz, J. et al. “Strengthening regional cooperation in the area of large pelagic fishery data collection (RECOLAPE)”, Annex III “Biological data collection for fisheries on highly migratory species” (2019).Boerder, K., Schiller, L. & Worm, B. Not all who wander are lost: Improving spatial protection for large pelagic fishes. Mar. Policy 105, 80–90 (2019).
    Google Scholar 
    Giakoumi, S. et al. Conserving European biodiversity across realms. Conserv. Lett. 12, e12586 (2019).
    Google Scholar 
    Gascuel, D. & Cheung, W. W. In Predicting Future Oceans 79–85 (Elsevier, 2019).Macias, D., Garcia-Gorriz, E. & Stips, A. Major fertilization sources and mechanisms for Mediterranean Sea coastal ecosystems. Limnol. Oceanogr. 63, 897–914 (2018).ADS 
    CAS 

    Google Scholar 
    Alvarez-Berastegui, D., Tugores, M., Ottmann, D., Martín-Quetglas, M. & Reglero, P. Bluefin tuna larval indices in the Western Mediterranean, ecological and analytical sources of uncertainty. Collect. Vol. Sci. Pap. ICCAT. 77, 289–311 (2020).
    Google Scholar 
    ICCAT. 2020 SCRS Advice to the Commission (Madrid, Spain, 2020).Clavel-Henry, M., Piroddi, C., Quattrocchi, F., Macias, D. & Christensen, V. Spatial distribution and abundance of mesopelagic fish biomass in the Mediterranean Sea. Front. Mar. Sci. 7, 1136 (2020).
    Google Scholar 
    García-Ruiz, C. et al. Spatio-temporal patterns of macrourid fish species in the northern Mediterranean Sea. Sci. Mar. 83, 117–127 (2019).
    Google Scholar 
    Ainsworth, C. Quantifying species abundance trends in the Northern Gulf of California using local ecological knowledge. Mar. Coast. Fish. 3, 190–218 (2011).
    Google Scholar 
    Morris, E. K. et al. Choosing and using diversity indices: Insights for ecological applications from the German Biodiversity Exploratories. Ecol. Evol. 4, 3514–3524 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    Coll, M. et al. Ecological indicators to capture the effects of fishing on biodiversity and conservation status of marine ecosystems. Ecol. Ind. 60, 947–962 (2016).
    Google Scholar 
    Swartz, W., Sala, E., Tracey, S., Watson, R. & Pauly, D. The spatial expansion and ecological footprint of fisheries (1950 to present). PLoS One 5, e15143 (2010).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Damasio, L. M., Peninno, M. G. & Lopes, P. F. Small changes, big impacts: Geographic expansion in small-scale fisheries. Fish. Res. 226, 105533 (2020).
    Google Scholar 
    Coll, M. et al. Assessing fishing and marine biodiversity changes using fishers’ perceptions: The Spanish Mediterranean and Gulf of Cadiz case study. PLoS One 9, e85670 (2014).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Tsikliras, A. C., Dinouli, A., Tsiros, V.-Z. & Tsalkou, E. The Mediterranean and Black Sea fisheries at risk from overexploitation. PLoS ONE 10, e0121188 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    Pittman, S. et al. Seascape ecology: Identifying research priorities for an emerging ocean sustainability science. Mar. Ecol. Prog. Ser. 663, 1–29 (2021).ADS 

    Google Scholar 
    Kritzer, J. P. & Liu, O. R. In Stock Identification Methods 29–57 (Elsevier, 2014).Piroddi, C., Heymans, J. J., Macias, D., Gregoire, M. & Townsend, H. Editorial: Using ecological models to support and shape environmental policy decisions. Front. Mar. Sci. https://doi.org/10.3389/fmars.2021.815313 (2021).
    Google Scholar 
    Macias, D. et al. JRC marine modelling framework in support of the marine strategy framework directive: Inventory of models, basin configurations and datasets. Update 2018. (2018).Piante, C. & Ody, D. Blue Growth in the Mediterranean Sea: The Challenge of Good Environmental Status. 192 (France, 2015).Borja, A. et al. Past and future grand challenges in marine ecosystem ecology. Front. Mar. Sci. 7, 362 (2020).
    Google Scholar 
    Claudet, J., Loiseau, C., Sostres, M. & Zupan, M. Underprotected marine protected areas in a global biodiversity hotspot. One Earth 2, 380–384 (2020).ADS 

    Google Scholar 
    Piroddi, C., Coll, M., Steenbeek, J., Moy, D. M. & Christensen, V. Modelling the Mediterranean marine ecosystem as a whole: Addressing the challenge of complexity. Mar. Ecol. Prog. Ser. 533, 47–65 (2015).ADS 

    Google Scholar 
    Walters, C., Pauly, D. & Christensen, V. Ecospace: Prediction of mesoscale spatial patterns in trophic relationships of exploited ecosystems, with emphasis on the impacts of marine protected areas. Ecosystems 2, 539–554 (1999).
    Google Scholar 
    Christensen, V., Walters, C., Pauly, D. & Forrest, R. Ecopath with Ecosim 6: A User’s Guide (University of British Columbia, 2008).
    Google Scholar 
    Kaschner, K. et al. AquaMaps: Predicted range maps for aquatic species. In World Wide Web Electronic Publication, www.aquamaps.org, Version, vol. 8, 2016 (2016).De Mutsert, K., Lewis, K. A., White, E. D. & Buszowski, J. End-to-End modeling reveals species-specific effects of large-scale coastal restoration on living resources facing climate change. Front. Mar. Sci. 8, 104 (2021).
    Google Scholar 
    Coll, M. et al. Advancing global ecological modeling capabilities to simulate future trajectories of change in marine ecosystems. Front. Mar. Sci. 741, 567877 (2020).
    Google Scholar 
    Shannon, C. & Weaver, W. (Univ. Illinois Press, 1949).Ainsworth, C. H. & Pitcher, T. J. Modifying Kempton’s species diversity index for use with ecosystem simulation models. Ecol. Ind. 6, 623–630 (2006).
    Google Scholar 
    Coll, M. & Steenbeek, J. Standardized ecological indicators to assess aquatic food webs: The ECOIND software plug-in for Ecopath with Ecosim models. Environ. Model. Softw. 89, 120–130 (2017).
    Google Scholar 
    Taconet, M., Kroodsma, D. & Fernandes, J. Global Atlas of AIS-Based Fishing Activity—Challenges and Opportunities (2021). More

  • in

    Analysis on ecological characteristics of Mississippian coral reefs in Langping, Guangxi

    Notwithstanding constraints on the amount of hard data, according to our integrated analysis, the developmental environment and ecology of reef communities have an important impact on the appearance of reefs.Analysis of environmental conditions for reef developmentSettings of reef developmentThe F/F extinction event in Late Devonian caused the complete recession of the reef-building communities based on stromatoporoid-coral assemblages7,17. The Carboniferous is generally considered to be a sub-optimal period for the development of framed reefs. After the biological mass extinction, microorganisms and algae rebuilt new reef-building ecosystems18,19. Some short-term biological frame reefs developed with low diversity, limited reef-building organisms, small sizes, and restricted distribution20. Harsh climate and marine conditions occurred in the Mississippian, including extensive marine hypoxia, repeated glacial and interglacial climate changes, and frequent changes of sea level and seawater surface temperature, potentially hindering the recovery of Early Carboniferous metazoan reefs7,21.Metazoans gradually began to participate in reef building in Early Viséan. A large number of biogenic structures formed by corals and bryozoans began to appear, including a small number of sponge reefs/mounds in the middle and late stage of Viséan. The richness and biodiversity of the Mississippian post-zoobenthic reefs flourished in the late Viséan during which corals, bryozoans, sponges, calcareous microorganisms, and some calcareous algae became the main builders3 and large-scale reefs could also be seen in some areas although most of the Viséan metazoan reefs were tabular or laminar. Thus, the metazoan skeletal reefs in the middle to late Viséan were considered to have been resurrected due to relatively warm climatic conditions and higher sea levels after a period of complete disintegration at the end of the Devonian and recession at the beginning of the Carboniferous7.Consequently, the coral reefs in the study area were the products of shallow benthic communities thriving in relatively favourable conditions of Late Viséan-Serpukhovian, which was common for reef development at that time7. Thus, it is expected that more synchronous reefs would to be identified in southern China, or even in the study area in the future.Paleogeography of reefsLangping is located in Dian-Qian-Gui Basin22 regionally (Fig. 2), in the eastern end of Tethys tectonic domain and at the interjunction of Tethys and Pacific structure globally. The Carboniferous Dian-Qian-Gui Basin is adjacent to the Tethys Basin. During the Early Carboniferous, the continent of Gondwana was close to the equator but was separated from the northern continent by the Tethys, where the tropical currents flowed freely from east to west. The benthic warm-water organisms were distributed widely with high abundance and diversity on both sides of the shallow shelf of Tethys.Figure 2Paleogeographic map of southern China in Viséan-Serpukhovian (modified from Feng23, Yao8, and Maillet24). This figure was obtained from articles by Feng23, Yao8 and Maillet24 respectively. The author modified the picture with CorelDRAW (version 2022, and the URL link: https://www.coreldraw.com/cn/). QG Qian-Gui Basin, DQGX Dian-Qian-Gui-Xiang platform.Full size imageViséan-Serpukhovian ecosystems experienced dramatic climate changes and widespread glaciation25. However, the Viséan was also a key layer for a variety of biological structures, with abundant coral reefs and a high diversity of shallow benthic communities, peaking in the late Viséan. Newly discovered post-faunal reefs in Tianlin were mainly formed in the late Viséan-Serpukhovian period, which coincided with frequent sea level fluctuations and possible glacial changes. It seems counterintuitive that tropical coral communities developed during glacial period. However, recent studies suggest that the persistent warm ocean currents on the platform helped some coral species survive from Carboniferous glacial events24. While other areas of symbiotic reefs were poorly developed, Tianlin may provide an ecological sanctuary for corals associated with ocean currents26.Sedimentation of reef developmentAccording to the regional geological structure, the slope model for Langping paleocarbonate platform was obviously different from that of steep slope platform margin, which could be directly affected by waves. Langping palaeo-platform could be regarded as one of the small blocks (block fault barrier) separated from a large platform (continental margin sea basin)13. The relative positions of these blocks were crucial for the emergence and growth of reefs.In situ development of mud-crystalline tuffs and muddy tuffs with weak hydrodynamic conditions is common in the Langping area, and evaporites are poorly developed. There were patch reefs and reef layers in different sizes in the wide intraclast beach, where obviously developed reef beach complexes were rare. The fragments of carbonate base broken by storm in the clastic beach haven’t been observed. The study area is considered to be gentle-slope open platform27,28 based on sedimentary characteristics. It suggests that the study area was far away from the margin of steep-slope platform that directly affected by waves, and more consistent with less energetic internal environments of gentle-slope platform.On the vast platform of Langping gentle slop, deep water lead to low water energy. While in the coastal area, the water energy was relatively strong, thus coarse-grained bioclastic beach and a small amount of point reef could be developed. The beaches were irregular-shaped due to long term transportation and reformation effects of waves and water flow, showing low and gentle slope angles. Dispersed reef-beach complexes at the platform margin slightly impacted inner-platform seawater and the water flows smoothly29.Therefore, it can be assumed that Langping reefs developed along the intertidal shallows of the terrace. The seawater around Langping carbonate platform in Late Viséan-Serpukhovian was relatively shallow while the water flow was strong. Remains of crinoids, brachiopods, a few foraminifera, and solitary corals were likely broken by strong currents, and deposited in situ with a small amount of gravels and lime-mud (Fig. 3). The clastic beach was unstable, suggesting large-scale wave-resistant structures could not be formed quickly30 due to insufficient cohesive and consolidating organisms. In addition, the circumferential impact of water in extensive terraces leads to mud-lime deposition, which is detrimental to most benthic organisms. However, bondstone was more likely to be formed by some binding algaes in the platform (Fig. 4). Therefore, neither the surrounding or the inner region of the platform could provide favourable living conditions for coral reefs to develop over for a long term. The gently sloping terrace environment of Lanping resulted in significant differences in growth size, wave resistance and reef-building capacity between corals in the study area and those on the edge of the steeply sloping terrace.Figure 3Clastic beaches in the Langping. Various clastic beaches developed in the study area. Diverse composition, fragmentation degree and sorting of the clast indicate different water conditions of formation. This figure is modified by the author from field photos with CorelDRAW (version 2022, and the URL link: https://www.coreldraw.com/cn/).Full size imageFigure 4Algal bondstone in the Langping. Bondstone formed by various algaes living in still water. Morphology of bondstone correlates water environment and deposition of mud. Vast algal bondstones indicate deep water and high deposition rate. This figure is modified by the author from field photos with CorelDRAW (version 2022, and the URL link: https://www.coreldraw.com/cn/).Full size imageAt the same time, the warm climate of the late Viséan-Serpukhovian, the good circulation of seawater around the Langping platform, and the abundant supply of oxygen and nutrients were a series of favourable conditions that facilitated the growth of reef-building corals, which led to uplifts being formed on clastic beach, including patch reefs and reef layers with certain sizes. These uplifts impeded waves and provided a protected nearshore environment, though they were much smaller than those developed at the steep-slope platform margin. The inhabitants on the beach could not resist strong waves. These rises were therefore known as reef-beach complexes and could only persist where waves and currents were mild28. They were essentially different from the framework coral reefs which developed on steep-slope platform margin that reflected changed hydrodynamic conditions, nutrient sources, reef sizes, and growth rates.Another potentially favourable factor in the study area could be the deeper water area in the gentle-slope sedimentary environment, which could provide more stable conditions and reduce the damaging effects of global glacial events and large scale sea level fluctuations on reef-building communities25. The frequent fault activities in Dian-Qian-Gui Basin caused the rise and fall of equivalent sea level. More influence of sea-level fluctuations and hydrodynamic conditions would be exerted on Langping platform due to its small size. Furthermore, reef growth promoted by reef-building communities would be frequently disturbed. The sediments displaying evidence of multicycle sedimentation, different components, and diversely fragile clasts in the study area provided direct evidence of frequently changing environment.Alternatively, the sedimentary environment of Langping platform provided conditions favorable for reef-building communities to develop and reefs to grow rapidly. These factors directly or indirectly determined the ecology of reef-building communities and the general appearance of reef development in the study area.Overall, the environmental factor is the primary factor affecting the overall development trend of reefs.Inferred ecological characteristics of reef communitiesResponse of reef-building corals to hydrodynamic conditionsHydrodynamic conditions are very important factors for reef development, which directly determine the abundance and distribution of each reef-building population and are key factors influencing sedimentation and reef growth, and was particularly evident at Langping. Evidence from the fossils suggested the reef-building corals were also changed in response (Table 1). The hydrodynamic condition changes during the development of reefs are inferred based on analysis of the vertical sediments and microfacies changes of coral reefs in the study area31. How these ancient reef-building corals adapted to hydrodynamic conditions was reconstructed combining the evolution of reef-building communities with the study.Table.1 General situation of reef-building coral population in Langping.Full size tableThe Xiadong coral reef started with colonization and expansion of Diphyphyllum on the bioclastic hard substrates32,33. They grew vertically into upright clusters (Fig. 5A) and were insensitive to more sediment in a relatively calm, turbid water environment34. The relatively dense clumped Siphonodendron and massive Lithostrotion (Fig. 5B) were better suited to the turbulent water environment, becoming dominant over time, with Diphyphyllum subordinate with the continuous increase of the water energy, as indicated by the characteristics of sediment particles from fine to coarse. After flourishing for a period, the Siphonodendron–Lithostrotion assemblage eventually waned, likely due to the failure to adapt to the increasing hydrodynamic conditions. Diphyphyllum had persisted combined with Syringopora, to maintain the growth of the reef. However, this assemblage subsequently declined as a result of strong hydrodynamic conditions and finally died out in response to continuous falling of sea level. Consequently, the reefs stopped developing.Figure 5Sketch of coral cluster with upright growing morphology. Most reef-building corals in Langping grow vertically into cluster colonies. This type of morphology is very favourable for corals to get more living space and is important to reef-building. (A) Cluster coral individuals grow uprightly with certain distance between each other. (B) Polygonal columnar coral individuals grow closely to resist strong water flow. This figure is made by the author with CorelDRAW (version 2022, and the URL link: https://www.coreldraw.com/cn/).Full size imageThe Longjiangdong multi-layer reef was composed of three relatively independent, flat reef layers, suggesting three distinct periods of reef development. Diverse species were identified in the reef, with colonial coral Diphyphyllum contributing greatly to reef growth. Diphyphyllum clusters colonized in patchy form on substrates composed of bioclasts or lithic gravels (Fig. 6A). The first reef-building process was brief, ending under high-energy water conditions after a period of growing (Fig. 6B). Subsequently the hydrodynamic conditions became weaker and favorable. Then Diphyphyllum once again flourished. Diphyphyllum clumps in the unit grew closely together in strong currents, with larger and more sparse individuals than in the lower units. A relatively low energy environment was formed between the Diphyphyllum clusters (Fig. 6C). Subsequently, Diphyphyllum could only grow in a limited area of suitability due to the disturbance of high-energy water brought about by short-term sea-level rise and fall. Afterwards, the environment became more favourable and Diphyphyllum expanded rapidly. As a result, the upper unit of Longjiangdong coral reef was formed, in which Diphyphyllum individuals were slightly larger than those in the first two units. Finally, because the kinetic energy of the water continued to weaken, the plaster deposition forced the whole coral reef to stop growing (Fig. 6D).Figure 6Micrographs of sediments in different positions of reef. (A) Calcareous bioclastic limestone, with biological particles accounting for about 70% of the debris. Abundant and diverse organisms indicate a medium-energy environment of the subtidal zone. Samples were taken from the bioclastic beach at the reef base. (B) Slightly larger bioclastics but lower biologic content than that in (A) suggest an increasing water energy. (C) Various bioclastic particles account for about 80% of the clastic particles contained in the calcareous bio-granular rock. The obviously small benthos indicate a low-energy environment in the subtidal zone barriered by the Diphyphyllum clusters. (D) Bioclastic grainstone is mainly composed of marl, with fine clastic particles (about 30%) and bedding. Low biomass indicates a low-energy environment of the subtidal zone. This figure is modified by the author with CorelDRAW (version 2022, and the URL link: https://www.coreldraw.com/cn/). Meaning of the letters in the figure: C crinoids, BF brachiopods, F foraminifera, B bryozoan, P pelletoid, MF mollusk shell fragment.Full size imageLongjiangdong patch reef started to develop in a relatively deep water environment. Diphyphyllum initially colonized and expanded in favorable conditions with the increase of water energy. Then the reef-builders transitioned from a single coral species to an assemblage of Diphyphyllum–Caninia–Lithostrotionella. These three coral species grew independently and contribute almost equally to the structure of the reef. However, the structure and function of the coral community were not yet stable enough. It was easily influenced by the weakening hydrodynamics and the increasing sedimentation, resulting in only small patch reefs.The Xinzhai layer reef was initialized by colonization and expansion of Lonsdaleia on bioclastic beach. Large coral clusters were formed in the presence of turbulent water. With the weakening of hydrodynamic conditions, an unknown branchlike organism and Antheria communities continued to develop separately in this area. Slender branchlike organisms expanded rapidly in these low-energy water environments until they were replaced by some individual corals as hydrodynamic energy increased. Each builder was short-lived in this layer reef, departing from the reef just at the beginning of colonization and expansion, due to rapidly changed hydrodynamic conditions.The evolution of reef-building corals in these four reefs indicated that both the coral assemblages and coral individuals would constantly adapt to the changing hydrodynamic conditions in Langping as sea level rose and fell. Although this was a reactive adjustment of coral populations in response to long-term environmental impacts, it was clearly positive for the building and development of coral reefs.Impact of disturbance on reef communitiesDisturbance is a relatively discontinuous event, which is ubiquitous in nature. It may indirectly affect the composition and population structure of reef communities by changing the environmental conditions, thus affect the structure and function of reef communities, even the evolution of the reef35. The major disturbances evident in these Mississippian framework reefs were associated with frequent changes of water flow, and drastic changes of climate and weather. These seem to be most obvious in the Langping platform due to its small size, with more frequent environmental influence evident on the reef communities in the study area.The most direct effect of disturbance events on coral reefs is the disruption of continuously evolving reef communities, which is common in coral reef studies. After the interruption caused by disturbances, some communities gradually recover due to the absence of continuous disturbance, or the dominant biota may be substituted by invading communities. The winner after interruption is decided by random factors to a large extent, in a ‘Competitive lottery’36. The conditions for the emergence of ‘Competitive lottery’ also include the need for species in a community to have similar abilities to invade discontinuities and to tolerate environmental conditions.Certainly, low-intensity disturbance does not necessarily produce discontinuity, but medium-intensity disturbance without discontinuity could directly impact on community species diversity. According to the ‘Moderate disturbance hypothesis’, moderate disturbance is conducive to a higher level of community diversity37. In environmental conditions with moderate intensity of disturbance, most species will not disappear entirely. The dominant pioneer species will also be restrained by disturbance to a certain extent, so large number of species can coexist, attaining the highest diversity35.The reef-builders in Langping are diverse compared with the Late Carboniferous reefs in Ziyun County10, which also developed in Dian-Qian-Gui Basin. More than 4 reef-building corals are identified in Xiadong reef, while 4 and 3 are in Xinzhai layer reef, Longjiangdong patch reef respectively. These reef-building corals, mostly Diphyphyllum, Lithostrotion, Siphonodendron and Lonsdaleia, were distributed irregularly in the reefs. Their ecological niche and function were likely similar and none of them was obviously dominant in the community (Fig. 7). This is in line with ‘Competitive lottery’ theory and the ‘Moderate disturbance hypothesis’.Figure 7Different species occupied the discontinuity surface irregularly. (A) Different reef-builders colonized and grew on the same hard substrate. (B) and (C) show detailed morphology of colony corals of (A). (D) Colony corals and a large number of individual corals grew together in a limited area, indicating equal colonization on the newly formed discontinuity surface. This figure is modified by the author from field photos with CorelDRAW (version 2022, and the URL link: https://www.coreldraw.com/cn/).Full size imageThe stability of a classical reef ecosystem includes the ability to withstand external disturbances and the ability to return to its original state once the disturbance is removed37,38. It is generally accepted that communities with high diversity are always more stable although ecosystem stability is not absolutely correlated to biodiversity35.There have been no reef-building corals with strong resistance and rapid recovery ability in the communities in Langping. None of these corals succeeded in developing into dominant species that can build reef shelves, which made the reefs in Langping mostly appear in the form of small patch reefs or reef layers. However, formation of the large reef in Xiadong Village, patch reef in Longjiangdong Village, and layer reef in Xinzhai Village were all related to their relatively high diversity of reef-building corals. Compared with the situation where only one reef-building organism dominated the Bianping large coral reef, Wengdao large phylloid algal reef and Ivanovia cf. manchurica patch reefs in Ziyun County10, Guizhou province, the different coral assemblages in Langping area could effectively adapt to changing hydrodynamic conditions and maintain reef growth.Species diversity increased by disturbance stabilized the ecosystemas shown during the construction of coral reefs in Langping.Effects of non-reef-builders on reef-building coralsBesides reef-building corals, there were a large number of reef-dwellers and off-reef organisms in the study area. Reef-dwellers referred to the species that didn’t directly contribute to reef growth in the community, mainly including various benthos and algaes39. Off-reef organisms are not part of the reef-building community, but also play an important role in participating in energy flow and providing organic matter to the reef ecosystem40.Common reef-dwelling organisms include crinoids, brachiopods, gastropods, various algae, foraminifera, bryozoans and individual corals. Crinoids were overwhelmingly dominant in numbers in the reef samples studied here.Carboniferous echinodermata in Guangxi Province reached its peak in Middle-to-Late Mississippian. In terms of amount and distribution, thick limestone with echinodermata debris in the carbonate platform were often dominated by crinoids41,42,43,44,45,46. The large number of crinoids in Langping excluded other metazoans and restricted the development of benthic reef-builders in Late Viséan-Serpukhovian in Langping, leading to poorly developed reef-building communities.Microorganisms and algaes had limited success in stablishing on the moving clastic beach in frequently disturbed water. There has not been obvious evidence of extensive “algal turf” in the coastal area of Langping platform. Only a few corals bonded by algal mats were observed47 (Fig. 8). In addition to their significant contribution to primary productivity, macroalgae were considered to play an important role in two aspects of coral reef ecosystems. One was to promote reef construction by its own binding and consolidation48,49. The other was to create a good condition for zoobenthos larvae to dwell and develop, thereby improving species diversity50. The limited productivity of algae in Langping constrained coral reef trophic inputs, which may then have limited populations of dependent metazoans. As a result, algaes and other metazoans were unable to achieve a variety of reef-building patterns, such as bonding, bounding, entanglement51,52. The reef framework in the study area was not stable in the presence of strong water flow, and the biological communities could not deal with frequent environmental changes, which were directly related to poor development of calcareous algae.Figure 8Micrographs of microbes and algaes. (A) Encrustations (indicated by black arrows) with distinct thickness around coral clusters formed by microbe and algal mats through bonding mud. The encrustations were formed before the clastic deposition (indicated by white arrows), showing the corals were living then. Microbes and algaes inside of the dense coral clusters had little impact on corals. (B) Single polarized micrograph showed clear and smooth boundaries of coral individuals without encrustation or drilling hole made by microbes or algaes. Few corals surrounded by bonding algaes could be observed in Langping, indicating that algaes were poorly developed between coral clusters. This figure is modified by the author from field photos with CorelDRAW (version 2022, and the URL link: https://www.coreldraw.com/cn/).Full size imageInfluence of coral morphology on reef developmentThe accumulation of reef structure had obvious impact on communities. Large reef structures could support abundance and diverse biota by modifying local environments and creating diverse conditions. Consequently the reef-building communities thrived between disturbances, stabilizing reef construction. In terms of large reef, the framework-building corals would play a key role in reef construction regardless of which kind of patterns was adopted. Therefore, reef-building corals with large size, rapid growth vertically, and strong resistance would become the biggest contributors to reef frame construction.The main reef-building corals in Langping were composed of Diphyphyllum, Lithostrotion, Siphonodendron, and Lonsdaleia, etc., being the dominant builders. These corals were similar in morphology such as cluster colony, thick and strong skeleton, and densely packed individuals (Fig. 9), which enabled them to resist water flow. At the same time, the upright colonies were adaptable to relatively calm water, being insensitive to mud deposition. The ecological characteristics of the Langping corals matched the gently sloping environment, the deep water environment and the rapidly changing energy of the currents. These cluster corals were able to colonize hard substrates and expand rapidly, thus altering the surrounding environment. The visible carbonate uplifts were formed with a large amount of benthos grouped into reef-building communities. These distinct uplifts constructed by coral clusters in different water conditions are composed of coral reefs of different sizes and appearance in the study area.Figure 9Main reef-building corals in the study area. (A) Diphyphyllum, (B) Lithostrotion, (C) Siphonodendron, (D) Lonsdaleia. (A) Rapidly grew clusters of main reef-building corals. The strong individuals are packed tightly when growing to support each other. This figure is modified by the author from field photos with CorelDRAW (version 2022, and the URL link: https://www.coreldraw.com/cn/).Full size imageThe complex and diverse local environments formed by large coral reefs can significantly increase benthic populations and improve reef species diversity. As a result, the nutrient flow in the community becomes complicated, and nutrients could be recycled effectively by reducing loss caused by water flow. Therefore, the overall productivity of large coral reef communities was always high. Complex trophic structure satisfied most of the benthos in the community with sufficient nutrients and inorganic salts.The morphology of reef-building corals in Langping enabled them to become predominant species in various water environments, which promoted the continued domed growth of coral reefs and facilitates the development of reef-building communities that form a variety of reefs. It suggests that the morphology of reef-building corals was a key prerequisite for reef development.In conclusion, coral reef communities are always constrained and influenced by environmental conditions. However, the ecology of the inhabitants is also an important factor in the formation of coral reefs. More

  • in

    Effect of marigold (Tagetes erecta L.) on soil microbial communities in continuously cropped tobacco fields

    Chen, X. L. et al. Effects of Meloidogyne incognitaon the fungal community in tobaccorhizosphere. Rev. Bras. Cienc. Solo. 46, e0210127 (2022).
    Google Scholar 
    Zhang, S. X. et al. Research progresses on continuous cropping obstacles of tobacco. Soils 47(5), 823–829 (2015).CAS 

    Google Scholar 
    Luo, J. Y. et al. Effects of soil salinity onrhizosphere soil microbes in transgenic Bt cotton fields. J. Integr. Agric. 16, 1624–1633 (2017).CAS 

    Google Scholar 
    Chaparro, J. M. et al. Manipulating the soil microbiome to increase soil health and plant fertility. Biol. Fertil. Soils 48, 489–499 (2012).
    Google Scholar 
    Newton, A., Begg, G. & Swanston, J. Deployment of diversity for enhanced crop function. Ann. Appl. Biol. 154, 309–322 (2009).
    Google Scholar 
    Li, X. G. et al. Effects of intercropping with Atractylodeslancea and application of bio-organic fertiliser on soil invertebrates, disease control and peanut productivity in continuouspeanut cropping field in subtropical China. Agrofor. Syst. 88, 41–52 (2014).
    Google Scholar 
    Ahmed, W. et al. Ralstonia solanacearum, a deadly pathogen: Revisiting the bacterial wilt biocontrol practices in tobacco and other Solanaceae. Rhizosphere 21, 100479 (2022).
    Google Scholar 
    Gómez-Rodrıguez, O., Zavaleta-Mejıa, E., Gonzalez-Hernandez, V., Livera-Munoz, M. & Cárdenas-Soriano, E. Allelopathyand microclimatic modification of intercropping with marigold on tomato early blight disease development. Field Crops Res. 83, 27–34 (2003).
    Google Scholar 
    Weidenhamer, J. D., Montgomery, T. M., Cipollini, D. F., Weston, P. A. & Mohney, B. K. Plandensity and rhizosphere chemistry: Does marigold root exudate composition respond to intra-and interspecific competition?. J. Chem. Ecol. 45(5–6), 525–533 (2019).CAS 
    PubMed 

    Google Scholar 
    Ploeg, A. T. Effects of selected marigold varieties on root-knot nematodes and tomato and melon yields. Plant Dis. 86(5), 505–508 (2002).PubMed 

    Google Scholar 
    Hooks, C. R., Wang, K. H., Ploeg, A. & McSorley, R. Using marigold (Tagetes spp.) as a cover crop to protect crops fromplant-parasitic nematodes. Appl. Soil Ecol. 46, 307–320 (2010).
    Google Scholar 
    Li, W., Xu, J., Chen, H. & Qi, Y. Phytochemicals and their biological activities of plants in tagetes l.-sciencedirect. Chin. Herbal Med. 4(2), 103–117 (2012).
    Google Scholar 
    Weidenhamer, J. D., Mohney, B. K., Shihada, N. & Rupasinghe, M. Spatial and temporal dynamics of root exudation: How important is heterogeneity in allelopathic interactions?. J. Chem. Ecol. 40(8), 940–952 (2014).CAS 
    PubMed 

    Google Scholar 
    Marotti, I. et al. Thiophene occurrence in different tagetes species: Agricultural biomasses as sources ofbiocidal substances. J. Sci. Food Agric. 90(7), 1210–1217 (2010).CAS 
    PubMed 

    Google Scholar 
    Barto, E. K. et al. The fungal fastlane: Common mycorrhizal networks extendbioactive zones of allelochemicals in soils. PLoS ONE 6, e27195 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Evenhuis, A., Korthals, G. & Molendijk, L. Tagetes patula as an effective catch crop forlong-term control of Pratylenchus penetrans. Nematology 6, 877–881 (2004).
    Google Scholar 
    Wu, W. T. et al. Effects of marigold-tobacco rotation on soil nematode community composition. Southwest China J. Agric. Sci. 32(2), 342–348 (2019).
    Google Scholar 
    Reynolds, L. B., Potter, J. W. & Ball-Coelho, B. R. Crop rotation with sp. is an alternative to chemical fumigation for control of root-lesion nematodes. Agron. J. 92(5), 957–966 (2000).
    Google Scholar 
    El-Hamawi, M., Youssef, M. & Zawam, H. S. Management of Meloidogyne incognita, the root-knot nematode, on soybean asaffected by marigold and sea ambrosia (damsisa) plants. J. Pest Sci. 77, 95–98 (2004).
    Google Scholar 
    Kumar, N., Krishnappa, K., Reddy, B., Ravichandra, N. & Karuna, K. Intercropping for the management of root-knotnematode, Meloidogyne incognitain vegetable-based cropping systems. Indian J. Nematol. 35, 46–49 (2005).
    Google Scholar 
    Zhang, J. et al. Crop rotation with marigold promotes soil bacterial structure to assist in mitigating clubroot Incidence in Chinese Cabbage. Plants 11(17), 2295 (2022).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Xia, T. Y. et al. Microbial diversity of tobacco rhizospheresoil in different growth stages of marigold-tobacco intercropping system. Southwest China J. Agric. Sci. 31(4), 680–686 (2018).
    Google Scholar 
    Wei, H. Y. et al. Effects of marigold diversified cropping with angelica on fungal community in soils. Plant Prot. 41(5), 69–74 (2015).MathSciNet 
    CAS 

    Google Scholar 
    Li, Y. et al. Intercropping with marigold promotes soil health and microbialstructure to assist in mitigating tobacco bacterial wilt. J. Plant Pathol. 102, 731–742 (2020).
    Google Scholar 
    Caporaso, J. G. et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl. Acad. Sci. 108, 4516–4522 (2011).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Edgar, R. C. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996–998 (2013).CAS 
    PubMed 

    Google Scholar 
    Wang, Q., Garrity, G. M., Tiedje, J. M. & Cole, J. R. Naive bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. MicroBiol. 73, 5261–5267 (2007).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).CAS 
    PubMed 

    Google Scholar 
    Irikiin, I. et al. Rhizobacterial community-level, sole carbon source utilization pattern aff ects the delay in the bacterial wilt of tomato grown in rhizobacterial community model system. Appl. Soil Ecol. 34(1), 27–32 (2006).
    Google Scholar 
    Wu, M. N. et al. Soil fungistasis and its relations to soil microbial composition and diversity: A case study of a series of soils with different fungistasis. J. Environ. Sci. 20(7), 871–877 (2008).CAS 

    Google Scholar 
    Mendes, L. W. et al. Soil-Borne microbiome: Linking diversity to function. Microb. Ecol. 70(1), 255–265 (2015).CAS 
    PubMed 

    Google Scholar 
    Jaiswal, A. K. et al. Linking the belowground microbial composition, diversity and activity to soilborne disease suppression and growth promotion of tomato amended with biochar. Sci. Rep. 7, 44382 (2017).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Raaijmakers, J. M. & Mazzola, M. Soil immune responses soil microbiomes may be harnessed for plant health. Science 352, 1392–1393 (2016).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Kušlienė, G., Rasmussen, J., Kuzyakov, Y. & Eriksen, J. Medium-term response of microbial community to rhizodeposits of white clover and ryegrass and tracing of active processes induced by 13C and 15N labelled exudates. Soil Biol. Biochem. 76, 22–33 (2014).
    Google Scholar 
    Mohammadi, K. Soil microbial activity and biomass as influenced by tillage and fertilization in wheat production. Am.-Eurasian J. Agric. Environ. Sci. 10, 330–337 (2011).
    Google Scholar 
    Wang, G. H. et al. Research progress of Acidobacteria ecology in soils. Biotechnol. Bull. 32(2), 14–20 (2016).
    Google Scholar 
    Wei, H., Wang, L., Hassan, M. & Xie, B. Succession of the functional microbial communities and the metabolic functions in maize straw composting process. Bioresour. Technol. 256, 333–341 (2018).CAS 
    PubMed 

    Google Scholar 
    Wang, Y., Liu, L., Yang, J., Duan, Y. & Zhao, Z. The diversity of microbial community and function varied in response to different agricultural residues composting. Sci. Total Environ. 715, 136983 (2020).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Glass, N. L., Schmoll, M., Cate, J. H. & Coradetti, S. Plant cell wall deconstruction by ascomycete fungi. Annu. Rev. Microbiol. 67, 477–498 (2013).CAS 
    PubMed 

    Google Scholar 
    Li, Y. et al. Linking soil fungal community structure and function to soil organic carbon chemical composition in intensively managed subtropical bamboo forests. Soil Biol. Biochem. 107, 19–31 (2017).CAS 

    Google Scholar 
    Martins, L. F., Kolling, D., Camassola, M., Dillon, A. J. & Ramos, L. P. Comparison of Penicillium echinulatumand Trichoderma reeseicellulases in relation to their activity against various cellulosic substrates. Bioresour. Technol. 99, 1417–1424 (2008).CAS 
    PubMed 

    Google Scholar  More

  • in

    Community context and pCO2 impact the transcriptome of the “helper” bacterium Alteromonas in co-culture with picocyanobacteria

    We aimed to understand the impact of changing pCO2 (400 vs. 800 ppm, representing current and projected year 2100 concentrations) on Prochlorococcus and Synechococcus and its effects on their interactions with the co-cultured heterotrophic “helper” bacterium Alteromonas sp. EZ55. Consistent with our previous research [7], EZ55 was more strongly affected by year 2100 pCO2 than any of the photoautotrophs in our study despite the primary dependence of the latter organisms’ metabolism on CO2. Strikingly, elevated pCO2 tended to reduce or eliminate the effect of co-culture on EZ55, with far fewer genes being significantly differentially transcribed relative to axenic EZ55 at the same pCO2. Thus, pCO2 strongly impacted the metabolic conversation between cyanobacteria and EZ55. Our detailed analysis of differentially regulated metabolic pathways suggested three mutually reinforcing mechanisms underlying this dynamic interaction: (i) pCO2 impacts on the release of ‘leaky’ cyanobacteria-derived metabolites, (ii) alteration of the dynamics of competition over inorganic nutrients between the co-cultured organisms, and (iii) modulation of bacterial and phytoplankton stress states. We explore each of these mechanisms in further detail below.Carbon cycling of “leaky” metabolites in co-cultureThe media we used for coculturing phytoplankton and bacteria contained no exogenous carbon sources; therefore, EZ55 was dependent on cyanobacterial exudates to grow, and it is likely that much of its changed transcription reflected changing availability of extracellular metabolites in the medium. The significant upregulation of carbon catabolism and transport genes as well as chemotaxis genes in co-cultures relative to axenic EZ55 supports the view that bacterial remineralization of cyanobacteria-secreted organic compounds is a driving force in these simple ecosystems. Additionally, changes in transcription of carbohydrate catabolism and transport genes provide clues as to which metabolites were being secreted under different experimental conditions (Fig. 5).Fig. 5: Proposed reconstruction of Alteromonas EZ55 ecophysiology.Reconstructions are shown for four different community contexts (axenic culture, or co-culture with Prochlorococcus MIT9312, Synechococcus WH8102, or Synechococcus CC9311) at 400 or 800 ppm pCO2, reflecting possible changes in the availability of C compounds, growth limiting factors, and stress conditions consistent with differential gene transcription observations. EZ55 image was obtained by cryoelectron microscopy from the sessions reported in Hennon et al. [7]. Background colors for each partner correspond to the bar colors in Fig. 3.Full size imageLike all oxygenic phototrophs, the cyanobacteria studied here fix carbon using the enzyme rubisco, which also catalyzes the undesirable photorespiration reaction leading to the production of 2PG instead of photosynthate. Phytoplankton in the field and in culture have been observed to excrete low molecular weight carboxylic acids including glycolate [39,40,41]. Photorespiratory glycolate is one of the most abundant sources of carbon in the oceans [38] and a preferred growth substrate for some marine heterotrophic bacteria [42]. Moreover the bacterial glcD gene for converting glycolate to glyoxylate is ubiquitously transcribed in the ocean [41, 43]. Although EZ55 lacks a specific transporter for glycolate, it can be taken up by the cell using the same transporters used for acetate and lactate uptake [44, 45], both of which were upregulated in co-culture conditions at 400 ppm (Fig. 3). Our data also showed differential regulation of enzymes involved in glycolate catabolism pathways, with at least one pathway upregulated in co-culture with each cyanobacterial strain (Fig. 3). We further demonstrated that EZ55 cultures were capable of growth on glycolate as a sole source of carbon, possibly using a novel GlcDF fusion protein (Fig. S11) and/or a plant-like LOX/GOX enzyme (Fig. 4). Thus, photorespiratory byproducts are likely a source of carbon for EZ55 in these cultures, particularly in the presence of MIT9312, which has no detectable enzymes for reclaiming 2PG on its own.There was also evidence that EZ55 utilized amino acids, organic acids, and fatty acids produced by phytoplankton under certain conditions in these cultures (Fig. S9). Lactate, acetate, and propanoate transporters and catabolism pathways were upregulated in co-culture with all cyanobacteria, as was pyruvate dehydrogenase with MIT9312, but only at 400 ppm. Both valine and glycine catabolism were also upregulated at 400 ppm in co-culture with the two Synechococcus strains, and fatty acid catabolism was upregulated in co-culture with MIT9312 and CC9311 at 400 ppm pCO2. Most of these substances have been directly or indirectly observed in cyanobacterial cultures in previous studies. For example, glycolate, lactate, acetate, and pyruvate have been directly measured in Prochlorococcus spent media [39], and co-culture with Prochlorococcus can fulfill the SAR11 growth requirement for glycine and pyruvate [46]. Fatty acid catabolism genes may have targeted membrane vesicles which are abundantly released by Prochlorococcus and other marine bacteria and may be a significant source of carbon for heterotrophs in the ocean [47, 48]; if so, future studies should investigate if WH8102 produces fewer vesicles than the other two cyanobacteria, explaining the differential transcription of beta-oxidation genes observed here.Valine, fatty acid, and propanoate catabolic pathways intersect with the formation of propanoyl-coA which in bacteria is generally fed into the TCA cycle through the methylcitrate pathway [49], which was significantly downregulated at 400 ppm in co-culture with all cyanobacteria even though other genes in these pathways were upregulated. Therefore, it is not clear what the ultimate fate of carbon from these sources is, although it is possible that EZ55 may be able to convert propanoyl-coA into a TCA cycle intermediate through another alternative pathway (e.g. as has been described in Mycobacterium tuberculosis via the methylmalonyl pathway [50]).Notably, gene transcription related to the utilization of all these products declined at 800 ppm pCO2 (Figs. 3, S8, S9). This was not unexpected for enzymes in the glycolate utilization pathways, as the increased CO2/O2 ratio at 800 ppm should decrease the rate of photorespiration relative to carbon fixation and therefore the availability of photorespiratory metabolites like glycolate [51, 52]. It is not clear, however, why organic and fatty acids would be less abundant in cyanobacterial exudates at 800 ppm. One possibility is that cyanobacteria release fewer of these compounds into the medium at high pCO2 because of a change in their internal redox state under these conditions favoring full oxidation of photosynthate. If future pCO2 conditions fundamentally alter the character of phytoplankton exudates, this could have profound implications for evolution and ecosystem functioning in future oceans.Evidence for inorganic nutrient limitation and competitionAutotrophic cyanobacteria and heterotrophic EZ55 were unlikely to compete over carbon under our experimental conditions, but we observed evidence of competition over inorganic nutrients such as N, P, and Fe. EZ55 phosphate, ammonium, and iron transporters, nitrogen regulatory protein P-II, and glutamine synthetase (the primary gateway for N assimilation in bacteria) were all more highly transcribed for all co-cultures compared to axenic cultures at 400 ppm pCO2 (Fig. S6), suggesting a switch from axenic carbon limitation to nutrient limitation in the presence of a continual supply of photosynthetically derived carbon (Fig. 5). On the other hand, few nutrient transporters were upregulated compared to axenic under 800 ppm pCO2. Although gene transcription data alone is not sufficient to conclude whether Alteromonas is limited by inorganic or organic nutrients, the reduced importance of nutrient acquisition suggests that EZ55 is carbon limited under these conditions just as it is in the absence of cyanobacteria.There were comparatively few species-specific changes in EZ55 nutrient transporter gene transcription. One example was an ammonium transporter, which was strongly upregulated in co-culture with both open ocean cyanobacteria (MIT9312 and WH8102) at 400 ppm pCO2. This may reflect a response to a comparatively high affinity for N in cyanobacteria adapted to the permanently oligotrophic open ocean, making them much stronger competitors for limiting N than coastal CC9311. N competition with EZ55 has been observed to increase the relative competitive fitness of Prochlorococcus vs. Synechococcus (coastal strain WH7803) in 3-way co-cultures [53]. In contrast, WH8102 appears to have higher N demand under 800 ppm pCO2, significantly upregulating a nitrate transporter and several genes related to urea utilization (Fig. S2). This may be explained by the enhanced transcription of carbon fixation genes and faster exponential growth rates observed in WH8102 at elevated pCO2, increasing N demand, and may indicate that WH8102 was C limited at 400 ppm.It is important to note that different N sources were provided in PEv medium (in which axenic EZ55 and MIT9312 co-cultures were grown) and SEv medium (in which CC9311 and WH8102 co-cultures were grown), with NH4+ in the former and NO3- in the latter. However, we do not think this difference can explain the observed changes in gene regulation, since EZ55 is capable of growth using either N source. It is interesting to note, however, that EZ55’s ammonium transporter was upregulated in both media types (Fig. S6), suggesting it may be benefitting from ammonium excreted by Synechococcus in SEv co-cultures.Impacts of co-culture and pCO2 on stress conditionsEZ55 showed less transcription of stress-related genes at 400 than 800 ppm pCO2, and also less evidence of stress in co-culture with any cyanobacterium than in axenic culture by itself. Nearly every gene in the EZ55 genome related to protection from H2O2 was downregulated in co-culture at 400 ppm, as were a suite of other stress-related genes (Fig. 2); on the other hand, many of these genes were significantly upregulated relative to axenic conditions at 800 ppm. Additionally, at 800 ppm there was a pronounced difference in EZ55 H2O2 defense gene transcription between cyanobacterial partners. As we described previously [7], both monofunctional catalases were downregulated at 800 ppm in co-culture with MIT9312, as were 2 of 3 alkylhydroperoxide reductase genes (although the third was significantly upregulated). In contrast, the monofunctional catalase genes were significantly upregulated in co-culture with WH8102 at 800 ppm. Elevated transcription of genes involved in the biosynthesis of glycine betaine, an osmoprotectant which has also been shown to function as an antioxidant [54, 55], provides further evidence for increased oxidative stress in co-culture with Synechococcus at 800 ppm in EZ55.Some indication of the mechanism behind EZ55’s changing stress level under co-culture and elevated pCO2 can be seen in the dynamics of three stress-related RNA polymerase sigma factors. Both rpoE and rpoH, responsible for controlling envelope and heat stress regulons, respectively, were downregulated at 400 ppm in co-culture relative to axenic and 800 ppm conditions; rpoE was significantly upregulated at 800 ppm pCO2. These trends are consistent with starvation-induced oxidative stress under both axenic and 800 ppm conditions, as discussed above. In contrast, rpoS was upregulated at 400 ppm pCO2, strongly so in co-culture with MIT9312. RpoS is a specialized sigma factor that accumulates under conditions of nutrient deprivation or as cells enter the stationary phase and serves to increase general stress resistance [56, 57]. For example, in Escherichia coli RpoS was shown to play a crucial role for survival during nitrogen deprivation [58]. While the decoupling of the transcription of oxidative stress genes like catalase from rpoS transcription was unexpected, rpoS trends are consistent with EZ55 being nutrient limited at 400 ppm pCO2 (Fig. S6) and with the upregulation of catalase in co-culture with MIT9312, but not WH8102 or CC9311, at 400 ppm (Fig. 2).In contrast to EZ55, differentially transcribed genes related to stress responses were rare in cyanobacteria at 800 ppm. While both MIT9312 and WH8102 had significant growth impairments at 800 ppm (Fig. S1), there was little evidence of a stress-specific gene transcription response in either strain. DNA mismatch repair genes were enriched as a group at 800 ppm in Prochlorococcus, although the only individual stress-related protein that was differentially transcribed was a HLI protein that was strongly downregulated at 800 ppm. No stress-related genes or gene sets were enriched in WH8102, and the small number of differentially transcribed stress genes in CC9311 (e.g., heat-shock and HLI proteins) were all downregulated at 800 ppm. This could indicate a dependence of both MIT9312 and WH8102 on their co-cultured EZ55 partner for protection, as neither of these cyanobacterial genomes contains catalase or several other stress-response genes common in heterotrophic bacteria. It could also indicate that they have different stress response mechanisms than those that have been characterized in heterotrophic bacteria; for instance, several hypothetical proteins of unknown function were differentially regulated in each cyanobacterium between the pCO2 conditions. Finally, it is possible that the stresses experienced by MIT9312 and WH8102 occurred in the initial days after transfer into fresh media (i.e., the significantly extended lag period observed for both), and were alleviated by the late log phase when the cultures were sampled for RNA sequencing.Summary overview of metabolic responsesWe have shown that the response to elevated pCO2 in our algal:bacterial co-cultures was driven more by interspecies interactions than by CO2-specific responses themselves. While it is important to note that we do not have direct culture-based evidence for some of these claims, we feel that gene transcription evidence is strong for several conclusions regarding the interactions in our cultures (Fig. 5).First, increased pCO2 appears to have fundamentally altered the amount and/or types of carbon compounds secreted by all three cyanobacterial strains examined, placing EZ55 into a stationary-phase metabolic state nearly indistinguishable to being in culture media with no added carbon source at all. We suggest that this is driven directly by the higher CO2:O2 ratio, which lowered the rate of photorespiration and subsequent release of 2PG and/or glycolate and indirectly may have reduced the amount of incompletely oxidized carbon released by cyanobacteria by changing the intracellular redox state [59]. Possibly because of the changing supply of carbon, EZ55 also appeared to transition away from a state of nutrient competition with its cyanobacterial partners, exemplified by decreased transcription of nutrient transporters at elevated pCO2 (Fig. S6).Second, co-culture at 400 ppm clearly reduced stress on EZ55 relative to either axenic growth or co-culture growth at 800 ppm, possibly due to the provision of a more reliable source of C as described above by the cyanobacterial partner under these conditions. In contrast, both MIT9312 and WH8102 clearly experienced elevated stress, potentially related to the changes in EZ55’s metabolism under these conditions. One of the major conclusions from our previous work [7] was the finding that EZ55 reduced catalase transcription at 800 ppm pCO2, eliminating the “helper” effect that Prochlorococcus depends on to grow in culture [13, 14]. In this work we see that the catalase response in co-culture with MIT9312 was opposite that in co-culture with the two Synechococcus strains. One possible explanation for this lies in the fact that MIT9312, unlike the other three strains in this study, did not possess a complete 2PG catabolism pathway and therefore likely excreted this product where it was subsequently catabolized by EZ55. We confirmed by genomic analysis (Figs. S10–S13) and culture experiments (Fig. 4) that EZ55 was able to grow on glycolate as a sole carbon source, and that its intracellular H2O2 concentration was elevated compared to growth on glucose. We suggest that more 2PG was secreted by MIT9312 at 400 ppm pCO2 due to the lower CO2:O2 ratio, and that growth on this carbon source increased EZ55’s internal oxidative stress load, resulting in higher transcription of H2O2 defenses such as catalase (Fig. 2). If true, this provides one possible explanation of why the “helper” relationship broke down at elevated pCO2 – by leaking 2PG as a readily available growth substrate for EZ55 at 400 ppm, MIT9312 forced EZ55 to maintain a high degree of intracellular ROS defense, leading to the well-characterized ability of EZ55 to cross-protect Prochlorococcus strains from the relatively lower H2O2 concentrations in the bulk environment, and allowing MIT9312 to eliminate two energetically costly enzymatic pathways. When higher pCO2 reduced the rate of photorespiration, EZ55’s need to produce excess catalase decreased, resulting in lower levels of protection, and concomitant growth impairments, for MIT9312.This is an example of how leaky Black Queen functions allow organisms like Prochlorococcus to streamline their metabolism while simultaneously creating stable interdependencies within their communities. However, it also shows how Black Queen-stabilized exchanges can break down. If our hypothesized relationship between pCO2 and catalase production is correct, then this system depends on the passive release of a metabolic by-product that evolved under a set of atmospheric pCO2 conditions that have been largely stable for thousands of years – but this leaves the system particularly vulnerable to the rapid changes in pCO2 currently taking place and may leave Prochlorococcus with no protection at all in the future ocean. If Prochlorococcus is outcompeted by less-streamlined competitors, this could reduce the overall efficiency of primary production in the open ocean gyres with possible positive feedbacks on CO2 accumulation in the atmosphere. Subsequent experiments should examine whether Prochlorococcus can overcome this imbalance through adaptive evolution quickly enough to avoid serious disruptions of its current niche.In conclusion, these results provide further support for the observation that axenic cultures do not provide a good window into the behavior of natural communities. The metabolism of Alteromonas sp. EZ55, a ubiquitous consumer in the ocean, was strongly dependent on its community context, and relatively subtle shifts in the chemical environment induced by elevated pCO2 were sufficient to significantly remodel its physiology. Moreover, the transcriptional response of EZ55 to changing pCO2 was much greater than that of any of the photoautotrophs examined, suggesting that more work is needed to understand the often-ignored heterotrophic bacteria associated with marine primary producers and how they will respond to global ocean change. Thus, further research is indicated on some of our core findings and hypotheses (e.g., the role of 2PG, and the nature of the carbon exchanged between the cyanobacteria and Alteromonas) via metabolomics or direct substrate measurements. These results further highlight the importance of laboratory experiments using co-cultures as an experimentally tractable intermediate between oversimplified axenic cultures and overly complicated natural communities. They also highlight the dominant role that primary producers play in determining the metabolism and interactions of the organisms that depend on them for sustenance. More

  • in

    Optimization of adult mosquito trap settings to monitor populations of Aedes and Culex mosquitoes, vectors of arboviruses in La Reunion

    Randolph, S. E. & Rogers, D. J. The arrival, establishment and spread of exotic diseases: Patterns and predictions. Nat. Rev. Microbiol. 8, 361–371 (2010).Article 
    PubMed 

    Google Scholar 
    Boussès, P., Dehecq, J. S., Brengues, C. & Fontenille, D. Inventaire actualisé des moustiques (Diptera : Culicidae) de l’île de La Réunion, océan Indien. Bulletin de la Société de pathologie exotique 106, 113–125 (2013).Article 
    PubMed 

    Google Scholar 
    Delatte, H. et al. Geographic distribution and developmental sites of Aedes albopictus (Diptera: Culicidae) during a Chikungunya epidemic event. Vector-Borne Zoonotic Dis. 8, 25–34 (2008).Article 
    PubMed 

    Google Scholar 
    Gomard, Y., Lebon, C., Mavingui, P. & Atyame, C. M. Contrasted transmission efficiency of Zika virus strains by mosquito species Aedes aegypti, Aedes albopictus and Culex quinquefasciatus from Reunion Island. Parasites Vectors https://doi.org/10.1186/s13071-020-04267-z (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Vazeille, M., Dehecq, J.-S. & Failloux, A.-B. Vectorial status of the Asian tiger mosquito Aedes albopictus of La Réunion Island for Zika virus: Ae. Albopictus of la réunion island. Med. Vet. Entomol. 32, 251–254 (2018).Article 
    PubMed 

    Google Scholar 
    Youssouf, H. et al. Rift valley fever outbreak, Mayotte, France, 2018–2019. Emerg. Infect. Dis. 26, 769–772 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Sang, R. et al. Rift valley fever virus epidemic in Kenya, 2006/2007: The entomologic investigations. Am. J. Trop. Med. Hyg. 83, 28–37 (2010).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Cardinale, E. et al. West Nile virus infection in horses, Indian ocean. Comp. Immunol. Microbiol. Infect. Dis. 53, 45–49 (2017).Article 
    PubMed 

    Google Scholar 
    Bouyer, J., Yamada, H., Pereira, R., Bourtzis, K. & Vreysen, M. J. B. Phased conditional approach for mosquito management using sterile insect technique. Trends Parasitol. 36, 325–336 (2020).Article 
    PubMed 

    Google Scholar 
    Lees, R. S., Carvalho, D. O. & Bouyer, J. Potential Impact of Integrating the Sterile Insect Technique into the Fight against Disease-Transmitting Mosquitoes 1081–1118 (CRC Press, 2021). https://doi.org/10.1201/9781003035572-33.Book 

    Google Scholar 
    Gouagna, L. C. et al. Strategic approach, advances, and challenges in the development and application of the SIT for area-wide control of Aedes albopictus mosquitoes in Reunion Island. Insects 11, 770 (2020).Article 
    PubMed Central 

    Google Scholar 
    Bouyer, J. & Lefrançois, T. Boosting the sterile insect technique to control mosquitoes. Trends Parasitol. 30, 271–273 (2014).Article 
    PubMed 

    Google Scholar 
    Soghigian, J. et al. Genetic evidence for the origin of Aedes aegypti, the yellow fever mosquito, in the southwestern Indian Ocean. Mol. Ecol. 29, 3593–3606 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Bouyer, J. & Vreysen, M. J. B. Yes, irradiated sterile male mosquitoes can be sexually competitive!. Trends Parasitol. 36, 877–880 (2020).Article 
    PubMed 

    Google Scholar 
    Owino, E. A. et al. Field evaluation of natural human odours and the biogent-synthetic lure in trapping Aedes aegypti, vector of dengue and chikungunya viruses in Kenya. Parasites Vectors 7, 451 (2014).
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kröckel, U., Andreas, R., Eiras, Á. & Geier, M. New tools for surveillance of adult yellow fever mosquitoes: Comparison of trap catches with human landing rates in an urban environment. J. Am. Mosq. Control Assoc. 22, 229–238 (2006).Article 
    PubMed 

    Google Scholar 
    Haramboure, M. et al. Modelling the control of Aedes albopictus mosquitoes based on sterile males release techniques in a tropical environment. Ecol. Model. 424, 109002 (2020).Article 

    Google Scholar 
    Farajollahi, A. et al. Field efficacy of BG-sentinel and industry-standard traps for Aedes albopictus (Diptera: Culicidae) and West Nile Virus Surveillance. J. Med. Entomol. 46, 919–925 (2009).Article 
    PubMed 

    Google Scholar 
    Roiz, D. et al. Trapping the Tiger: Efficacy of the novel BG-sentinel 2 with several attractants and carbon dioxide for collecting Aedes albopictus (Diptera: Culicidae) in Southern France. J. Med. Entomol. 53, 460–465 (2016).Article 
    PubMed 

    Google Scholar 
    Wilke, A. B. B. et al. Assessment of the effectiveness of BG-sentinel traps baited with CO2 and BG-Lure for the surveillance of vector mosquitoes in miami-dade County Florida. PLoS ONE 14, e0212688 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Staunton, K. M. et al. Effect of BG-lures on the male aedes (Diptera: Culicidae) sound trap capture rates. J. Med. Entomol. 58, 2425–2431 (2021).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Visser, T. M. et al. Optimisation and field validation of odour-baited traps for surveillance of Aedes aegypti adults in Paramaribo Suriname. Parasites Vectors 13, 121 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Owino, E. A. et al. An improved odor bait for monitoring populations of Aedes aegypti-vectors of dengue and chikungunya viruses in Kenya. Parasites Vectors 8, 253 (2015).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Le Goff, G. et al. Comparison of efficiency of BG-sentinel traps baited with mice, mouse-litter, and CO2 lures for field sampling of male and female aedes albopictus mosquitoes. Insects 8, 95 (2017).Article 
    PubMed Central 

    Google Scholar 
    Nielsen, G. D., Petersen, S. H., Vinggaard, A. M., Hansen, L. F. & Wolkoff, P. Ventilation, CO2 production, and CO2 exposure effects in conscious, restrained CF-1 mice. Pharmacol. Toxicol. 72, 163–168 (1993).
    Article 
    PubMed 

    Google Scholar 
    Gouagna, L. C., Dehecq, J.-S., Fontenille, D., Dumont, Y. & Boyer, S. Seasonal variation in size estimates of Aedes albopictus population based on standard mark–release–recapture experiments in an urban area on Reunion Island. Acta Trop. 143, 89–96 (2015).Article 
    PubMed 

    Google Scholar 
    Dekker, T., Geier, M. & Cardé, R. T. Carbon dioxide instantly sensitizes female yellow fever mosquitoes to human skin odours. J. Exp. Biol. 208, 2963–2972 (2005).Article 
    PubMed 

    Google Scholar 
    Grant, A. J. & O’Connell, R. J. Age-related changes in female mosquito carbon dioxide detection. J. Med. Entomol. 44, 617–623 (2007).Article 
    PubMed 

    Google Scholar 
    Bohbot, J. & Vogt, R. G. Antennal expressed genes of the yellow fever mosquito (Aedes aegypti L.); characterization of odorant-binding protein 10 and takeout. Insect Biochem. Mol. Biol. 35, 961–979 (2005).Article 
    PubMed 

    Google Scholar 
    Hartberg, W. K. Observations on the mating behaviour of Aedes aegypti in nature. Bull. World Health Organ. 45, 847 (1971).PubMed 
    PubMed Central 

    Google Scholar 
    Cator, L. J., Arthur, B. J., Ponlawat, A. & Harrington, L. C. Behavioral observations and sound recordings of free-flight mating swarms of Ae. aegypti (Diptera: Culicidae) in Thailand. J. Med. Entomol. 48, 941–946 (2011).Article 
    PubMed 

    Google Scholar 
    Lacroix, R., Delatte, H., Hue, T. & Reiter, P. Dispersal and survival of male and female Aedes albopictus(Diptera: Culicidae) on Réunion Island. J. Med. Entomol. 46, 1117–1124 (2009).Article 
    PubMed 

    Google Scholar 
    Pombi, M. et al. Field evaluation of a novel synthetic odour blend and of the synergistic role of carbon dioxide for sampling host-seeking Aedes albopictus adults in Rome, Italy. Parasites Vectors 7, 580 (2014).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Cilek, J. E., Hallmon, C. F. & Johnson, R. Semi-field comparison of the Bg Lure, nonanal, and 1-Octen-3-OL to attract adult mosquitoes in northwestern Florida. J. Am. Mosq. Control Assoc. 27, 393–397 (2011).Article 
    PubMed 

    Google Scholar 
    Bagny Beilhe, L., Delatte, H., Juliano, S. A., Fontenille, D. & Quilici, S. Ecological interactions in Aedes species on Reunion Island. Med. Vet. Entomol. 27, 387–397 (2013).Article 
    PubMed 

    Google Scholar 
    Golstein, C., Boireau, P. & Pagès, J.-C. Benefits and limitations of emerging techniques for mosquito vector control. Comptes Rendus Biol. 342, 270–272 (2019).Article 

    Google Scholar 
    Maïga, H., Gilles, J. R. L., Lees, R. S., Yamada, H. & Bouyer, J. Demonstration of resistance to satyrization behavior in Aedes aegypti from La Réunion island. Parasite 27, 22 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Zeileis, A., Kleiber, C. & Jackman, S. Regression models for count data in R. J. Stat. Soft. https://doi.org/10.18637/jss.v027.i08 (2008).Article 

    Google Scholar 
    Fawaz, E. Y., Allan, S. A., Bernier, U. R., Obenauer, P. J. & Diclaro, J. W. Swarming mechanisms in the yellow fever mosquito: Aggregation pheromones are involved in the mating behavior of Aedes aegypti. J. Vector Ecol. 39, 347–354 (2014).Article 
    PubMed 

    Google Scholar 
    Guthery, F. S., Burnham, K. P. & Anderson, D. R. Model selection and multimodel inference: A practical information-theoretic approach. J. Wildl. Manag. 67, 655 (2003).Article 

    Google Scholar 
    Manly, B. F. J. Randomization, Bootstrap and Monte Carlo Methods in Biology 399 (CRC Press/Chapman & Hall, 2006). https://doi.org/10.1201/9781315273075.Book 
    MATH 

    Google Scholar 
    R Core Team. R: A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, 2022).Barton, K. MuMIn: Multi-Model Inference. (R-Forge, 2022).
    Google Scholar 
    Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach 496 (Springer-Verlag, 2002).MATH 

    Google Scholar 
    Xie, Y., Dervieux, C. & Riederer, E. R Markdown Cookbook (Chapman; Hall/CRC, 2020). https://doi.org/10.1201/9781003097471.Book 

    Google Scholar  More

  • in

    Lithology and disturbance drive cavefish and cave crayfish occurrence in the Ozark Highlands ecoregion

    Sket, B. Can we agree on an ecological classification of subterranean animals?. J. Nat. Hist. 42, 1549–1563. https://doi.org/10.1080/00222930801995762 (2008).Article 

    Google Scholar 
    Mammola, S. et al. Scientists’ warning on the conservation of subterranean ecosystems. Bioscience 69, 641–650. https://doi.org/10.1093/biosci/biz064 (2019).Article 

    Google Scholar 
    Boulton, A. J., Fenwick, G. D., Hancock, P. J. & Harvey, M. S. Biodiversity, functional roles and ecosystem services of groundwater invertebrates. Invertebr. Syst. 22, 103–116. https://doi.org/10.1071/IS07024 (2008).Article 

    Google Scholar 
    Danielopol, D. L. & Griebler, C. Changing paradigms in groundwater ecology—From the ‘living fossils’ tradition to the ‘new groundwater ecology’. Int. Rev. Hydrobiol. 93, 565–577. https://doi.org/10.1002/iroh.200711045 (2008).Article 

    Google Scholar 
    Griebler, C., Malard, F. & Lefébure, T. Current developments in groundwater ecology—From biodiversity to ecosystem function and services. Curr. Opin. Biotechnol. 27, 159–167. https://doi.org/10.1016/j.copbio.2014.01.018 (2014).Article 
    PubMed 

    Google Scholar 
    Fišer, C. Niphargus—A model system for evolution and ecology. In Encyclopedia of Caves (eds Culver, D. C. et al.) 746–755 (Academic Press, 2019).Chapter 

    Google Scholar 
    Riddle, M. R. et al. Insulin resistance in cavefish as an adaptation to a nutrient-limited environment. Nature 555, 647–651. https://doi.org/10.1038/nature26136 (2018).Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Gibert, J. et al. Assessing and conserving groundwater biodiversity: Synthesis and perspectives. Freshw. Biol. 54, 930–941. https://doi.org/10.1111/j.1365-2427.2009.02201.x (2009).Article 

    Google Scholar 
    Trontelj, P. et al. A molecular test for cryptic diversity in ground water: How large are the ranges of macro stygobionts?. Freshw. Biol. 54, 727–744. https://doi.org/10.1111/j.1365-2427.2007.01877.x (2009).Article 

    Google Scholar 
    Cooper, J. E. Ecological and Behavioral Studies in Shelta Cave, Alabama, with Emphasis on Decapod Crustaceans (University of Kentucky, 1975).
    Google Scholar 
    Voituron, Y., de Fraipont, M., Issartel, J., Guillaume, O. & Clobert, J. Extreme lifespan of the human fish (Proteus anguinus): A challenge for ageing mechanisms. Biol. Lett. 7, 105–107. https://doi.org/10.1098/rsbl.2010.0539 (2011).Article 
    PubMed 

    Google Scholar 
    Poulson, T. L. Cave adaptation in amblyopsid fishes. Am. Midl. Nat. 70, 257–290. https://doi.org/10.2307/2423056 (1963).Article 

    Google Scholar 
    Venarsky, M. P., Huryn, A. D. & Benstead, J. P. Re-examining extreme longevity of the cave crayfish Orconectes australis using new mark–recapture data: A lesson on the limitations of iterative size-at-age models. Freshw. Biol. 57, 1471–1481. https://doi.org/10.1111/j.1365-2427.2012.02812.x (2012).Article 

    Google Scholar 
    Culver, D. C., Kane, T. C. & Fong, D. W. Adaptation and Natural Selection in Caves: The Evolution of Gammarus minus (Harvard University Press, 1995).Book 

    Google Scholar 
    Niemiller, M. L. & Poulson, T. L. Subterranean fishes of North America: Amblyopsidae. In Biology of Subterranean Fishes (eds Trajano, E. et al.) 169–280 (CRC Press, 2010).Chapter 

    Google Scholar 
    Fišer, C., Zagmajster, M. & Zakšek, V. Coevolution of life history traits and morphology in female subterranean amphipods. Oikos 122, 770–778. https://doi.org/10.1111/j.1600-0706.2012.20644.x (2013).Article 

    Google Scholar 
    Purvis, A., Gittleman, J. L., Cowlishaw, G. & Mace, G. M. Predicting extinction risk in declining species. Proc. Biol. Sci. 267, 1947–1952. https://doi.org/10.1098/rspb.2000.1234 (2000).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Pearson, R. G. et al. Life history and spatial traits predict extinction risk due to climate change. Nat. Clim. Change 4, 217–221. https://doi.org/10.1038/nclimate2113 (2014).Article 
    ADS 

    Google Scholar 
    Niemiller, M. L., Bichuette, E. & Taylor, S. J. Conservation of cave fauna in Europe and the Americas. In Ecological Studies: Cave Ecology (eds Moldovan, O. T. et al.) 451–478 (Springer, 2018).Chapter 

    Google Scholar 
    Niemiller, M. L. & Taylor, S. J. Protecting cave life. In Encyclopedia of Caves (eds Culver, D. C. et al.) 822–829 (Academic Press, 2019).Chapter 

    Google Scholar 
    Niemiller, M. L., Taylor, S. J., Slay, M. E. & Hobbs, H. H. III. Biodiversity in the United States and Canada. In Encyclopedia of Caves (eds Culver, D. C. et al.) 163–176 (Academic Press, 2019).Chapter 

    Google Scholar 
    Hortal, J. et al. Seven shortfalls that beset large-scale knowledge of biodiversity. Annu. Rev. Ecol. Evol. Syst. 46, 523–529. https://doi.org/10.1146/annurev-ecolsys-112414-054400 (2015).Article 

    Google Scholar 
    MacKenzie, D. I. et al. Occupancy Estimation and Modeling: Inferring Patterns and Dynamics of Species Occurrence (Academic Press, 2018).MATH 

    Google Scholar 
    Roberto, P. & Pietro, B. Species rediscovery or lucky endemic? Looking for the supposed missing species Leistus punctatissimus through a biogeographer’s eye (Coleoptera, Carabidae). ZooKeys 740, 97–108. https://doi.org/10.3897/zookeys.740.23495 (2018).Article 

    Google Scholar 
    Chu, C., Mandrak, N. E. & Minns, C. K. Potential impacts of climate change on the distributions of several common and rare freshwater fishes in Canada. Divers. Distrib. 11, 299–310. https://doi.org/10.1111/j.1366-9516.2005.00153.x (2005).Article 

    Google Scholar 
    Larson, E. R. & Olden, J. D. Latent extinction and invasion risk of crayfishes in the southeastern United States. Conserv. Biol. 24, 1099–1110. https://doi.org/10.1111/j.1523-1739.2010.01462.x (2010).Article 
    PubMed 

    Google Scholar 
    Filipe, A. F. et al. Selection of priority areas for fish conservation in Guadiana River Basin, Iberian Peninsula. Conserv. Biol. 18, 189–200. https://doi.org/10.1111/j.1523-1739.2004.00620.x (2004).Article 

    Google Scholar 
    Mammola, S. et al. Fundamental research questions in subterranean biology. Biol. Rev. 95, 1855–1872. https://doi.org/10.1111/brv.12642 (2020).Article 
    PubMed 

    Google Scholar 
    Domínguez-Domínguez, O., Martínez-Meyer, E., Zombrano, L. & de León, G. P. Using ecological-niche modeling as a conservation tool for freshwater species: Live-bearing fishes in central Mexico. Conserv. Biol. 20, 1730–1739. https://doi.org/10.1111/j.1523-1739.2006.00588.x (2006).Article 
    PubMed 

    Google Scholar 
    Mammola, S. & Leroy, B. Applying species distribution models to caves and other subterranean habitats. Ecography 41, 1194–1208. https://doi.org/10.1111/ecog.03464 (2018).Article 

    Google Scholar 
    Castellarini, F., Malard, F., Dole-Olivier, M. & Gibert, J. Modelling the distribution of stygobionts in the Jura Mountains (eastern France). Implications for the protection of ground waters. Divers. Distrib. 13, 213–224. https://doi.org/10.1111/j.1472-4642.2006.00317.x (2007).Article 

    Google Scholar 
    Foulquier, A., Malard, F., Lefébure, T., Douady, C. J. & Gibert, J. The imprint of Quaternary glaciers on the present-day distribution of the obligate groundwater amphipod Niphargus virei (Niphargidae). J. Biogeogr. 35, 552–564. https://doi.org/10.1111/j.1365-2699.2007.01795.x (2008).Article 

    Google Scholar 
    Johns, T. et al. Regional-scale drivers of groundwater faunal distributions. Freshw. Sci. 34, 316–328. https://doi.org/10.1086/678460 (2015).Article 

    Google Scholar 
    Camp, C. D., Wooten, J. A., Jensen, J. B. & Bartek, D. F. Role of temperature in determining relative abundance in cave twilight zones by two species of lungless salamander (family Plethodontidae). Can. J. Zool. 92, 119–127. https://doi.org/10.1139/cjz-2013-0178 (2014).Article 

    Google Scholar 
    Korbel, K. L., Hancock, P. J., Serov, P., Lim, R. P. & Hose, G. C. Groundwater ecosystems vary with land use across a mixed agricultural landscape. J. Environ. Qual. 42, 380–390. https://doi.org/10.2134/jeq2012.0018 (2013).Article 
    PubMed 

    Google Scholar 
    Español, C. et al. Does land use impact on groundwater invertebrate diversity and functionality in floodplains?. Ecol. Eng. 103, 394–403. https://doi.org/10.1016/j.ecoleng.2016.11.061 (2017).Article 

    Google Scholar 
    Christman, M. C. et al. Predicting the occurrence of cave-inhabiting fauna based on features of the earth surface environment. PLoS One 11, e0160408. https://doi.org/10.1371/journal.pone.0160408 (2016).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Zagmajster, M. et al. Geographic variation in range size and beta diversity of groundwater crustaceans: Insights from habitats with low thermal seasonality. Glob. Ecol. Biogeogr. 23, 1135–1145. https://doi.org/10.1111/geb.12200 (2014).Article 

    Google Scholar 
    Poff, N. L. Landscape filters and species traits: Towards mechanistic understanding and prediction in stream ecology. J. North Am. Benthol. Soc. 16, 391–409. https://doi.org/10.2307/1468026 (1997).Article 

    Google Scholar 
    Stevenson, R. J. Scale-dependent determinants and consequences of benthic algal heterogeneity. J. North Am. Benthol. Soc. 16, 248–262. https://doi.org/10.2307/1468255 (1997).Article 
    ADS 

    Google Scholar 
    U.S. Geological Survey. NLCD 2011 land cover. Multi-Resolution Land Characteristics. https://www.mrlc.gov/data/nlcd-2011-land-cover-conus (2011).Adamski, J. C. Geochemistry of the Springfield Plateau Aquifer of the Ozark Plateaus Province in Arkansas, Kansas, Missouri and Oklahoma, USA. Hydrol. Process. 14, 849–866. https://doi.org/10.1002/(SICI)1099-1085(20000415)14:5%3c849::AID-HYP973%3e3.0.CO;2-7 (2000).Article 
    ADS 

    Google Scholar 
    Woods, A. J. et al. Ecoregions of Oklahoma (Color Poster with Map, Descriptive Text, Summary Tables, and Photographs) (U.S. Geological Survey, 2005).
    Google Scholar 
    Unklesbay, A. G. & Vineyard, J. D. Missouri Geology: Three Billion Years of Volcanoes, Seas, Sediments, and Erosion (University of Missouri Press, 1992).
    Google Scholar 
    Eigenmann, C. H. A new blind fish. In Proceedings of the Indiana Academy of Science 1897 (ed Waldo, C. A.) 231 (1898).Graening, G. O., Fenolio, D. B., Niemiller, M. L., Brown, A. V. & Beard, J. B. The 30-year recovery effort for the Ozark cavefish (Amblyopsis rosae): Analysis of current distribution, population trends, and conservation status of this threatened species. Environ. Biol. Fish. 87, 55–88. https://doi.org/10.1007/s10641-009-9568-2 (2010).Article 

    Google Scholar 
    Niemiller, M. L., Near, T. J. & Fitzpatrick, B. M. Delimiting species using multilocus data: Diagnosing cryptic diversity in the southern cavefish, Typhlichthys subterraneus (Teleostei: Amblyopsidae). Evolution 66, 846–866. https://doi.org/10.1111/j.1558-5646.2011.01480.x (2012).Article 
    PubMed 

    Google Scholar 
    Hobbs, H. H. Jr. & Brown, A. V. A new troglobitic crayfish from northwestern Arkansas (Decapoda: Cambaridae). Proc. Biol. Soc. Wash. 100, 1040–1048 (1987).
    Google Scholar 
    Graening, G. O., Slay, M. E., Brown, A. V. & Koppelman, J. B. Status and distribution of the endangered Benton cave crayfish, Cambarus aculabrum (Decapoda: Cambaridae). Southwest. Nat. 51, 376–381. https://doi.org/10.1894/0038-4909(2006)51[376:SADOTE]2.0.CO;2 (2006).Article 

    Google Scholar 
    Faxon, W. Cave animals from southwestern Missouri. Bull. Mus. Comp. Zool. 17, 225–240 (1889).
    Google Scholar 
    Graening, G. O., Hobbs, H. H. III., Slay, M. E., Elliott, W. R. & Brown, A. V. Status update for bristly cave crayfish, Cambarus setosus (Decapoda: Cambaridae), and range extension into Arkansas. Southwest. Nat. 51, 382–392. https://doi.org/10.1894/0038-4909(2006)51[382:SUFBCC]2.0.CO;2 (2006).Article 

    Google Scholar 
    Hobbs, H. H. III. Cambarus (Jugicambarus) subterraneus, a new cave crayfish (Decapoda: Cambaridae) from northeastern Oklahoma, with a key to the troglobitic members of the subgenus Jugicambarus. Proc. Biol. Soc. Wash. 106, 719–727 (1993).
    Google Scholar 
    Graening, G. O. & Fenolio, D. B. Status update of the Delaware County cave crayfish, Cambarus subterraneus (Decapoda: Cambaridae). Proc. Okla. Acad. Sci. 85, 85–89 (2005).
    Google Scholar 
    Hobbs, H. H. Jr. & Cooper, M. R. A new troglobitic crayfish from Oklahoma (Decapoda: Astacidae). Proc. Biol. Soc. Wash. 85, 49–56 (1972).
    Google Scholar 
    Graening, G. O. et al. Range extension and status update for the Oklahoma cave crayfish, Cambarus tartarus (Decapoda: Cambaridae). Southwest. Nat. 51, 94–99 (2006).Article 

    Google Scholar 
    Hobbs, H. H. III. A new cave crayfish of the genus Orconectes, subgenus Orconectes, from southcentral Missouri, USA, with a key to the stygobitic species of the genus (Decapoda, Cambaridae). Crustaceana 74, 635–646. https://doi.org/10.1163/156854001750377911 (2001).Article 

    Google Scholar 
    Miller, B. V. The Hydrology of the Carroll Cave-Toronto Springs System: Identifying and Examining Source Mixing Through Dye Tracing, Geochemical Monitoring, Seepage Runs, and Statistical Methods (Western Kentucky University, 2010).
    Google Scholar 
    Mouser, J. B., Brewer, S. K., Niemiller, M. L., Mollenhauer, R. & Van Den Bussche, R. Comparing visual and environmental DNA surveys for detection of stygobionts. Subterr. Biol. 39, 79–105. https://doi.org/10.3897/subtbiol.39.64279 (2021).Article 

    Google Scholar 
    Longmire, J. L., Maltbie, M. & Baker, R. J. Use of “Lysis Buffer” in DNA Isolation and Its Implication for Museum Collections (Museum of Texas Tech University, 1997).Book 

    Google Scholar 
    Mouser, J. B., Mollenhauer, R. & Brewer, S. K. Relationships between landscape constraints and a crayfish assemblage with consideration of competitor presence. Divers. Distrib. 25, 61–73. https://doi.org/10.1111/ddi.12840 (2019).Article 

    Google Scholar 
    U.S. Geological Survey. 1 Arc-second digital elevation models (DEMs)—USGS national map 3DEP downloadable data collection. https://data.usgs.gov/datacatalog/data/USGS:35f9c4d4-b113-4c8d-8691-47c428c29a5b (U.S. Geological Survey, 2017).Oak Ridge National Laboratory Distributed Active Archive Center. MODIS and VIIRS land products global subsetting and visualization tool. Oak Ridge National Laboratory Distributed Active Archive Center. https://doi.org/10.3334/ORNLDAAC/1379 (2018).Horton, J. D., San Juan, C. A. & Stoeser, D. B. The state geologic map compilation (SGMC) geodatabase of the conterminous United States. U.S. Geol. Surv. https://doi.org/10.3133/ds1052 (2017).Article 

    Google Scholar 
    MacKenzie, D. I. et al. Estimating site occupancy rates when detection probabilities are less than one. Ecology 83, 2248–2255. https://doi.org/10.1890/0012-9658(2002)083[2248:ESORWD]2.0.CO;2 (2002).Article 

    Google Scholar 
    Tyre, A. J. et al. Improving precision and reducing bias in biological surveys: Estimating false negative error rates. Ecol. Appl. 13, 1790–1801. https://doi.org/10.1890/02-5078 (2003).Article 

    Google Scholar 
    Gelman, A. & Hill, J. Data Analysis Using Regression and Multilevel Hierarchical Models (Cambridge University Press, 2007).
    Google Scholar 
    Kéry, M. & Royle, J. A. Applied Hierarchical Modeling in Ecology: Analysis of Distribution, Abundance and Species Richness in R and BUGS (Academic Press, 2016).MATH 

    Google Scholar 
    Plummer, M. JAGS: A program for analysis of Bayesian graphical models using Gibbs sampling. In Proceedings of the 3rd International Workshop on Distributed Statistical Computing (eds Hornik, K. et al.) 1–10 (Austrian Science Foundation, 2003).
    Google Scholar 
    R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2020).
    Google Scholar 
    Kellner, J. jagsUI: A wrapper around ‘rjags’ to streamline ‘JAGS’ analyses. https://CRAN.R-project.org/package=jagsUI (R-project, 2019).Brooks, S. P. & Gelman, A. General methods for monitoring convergence of iterative simulations. J. Comput. Graph. Stat. 7, 434–455. https://doi.org/10.1080/10618600.1998.10474787 (1998).Article 
    MathSciNet 

    Google Scholar 
    Kruschke, J. K. Doing Bayesian Data Analysis: A Tutorial with R, JAGS, and Stan (Academic Press, 2015).MATH 

    Google Scholar 
    Hobbs, N. T. & Hooten, M. B. Bayesian Models (Princeton University Press, 2015). https://doi.org/10.1515/9781400866557.Book 

    Google Scholar 
    Conn, P. B., Johnson, D. S., Williams, P. J., Melin, S. R. & Hooten, M. B. A guide to Bayesian model checking for ecologists. Ecol. Monogr. 88, 526–542. https://doi.org/10.1002/ecm.1314 (2018).Article 

    Google Scholar 
    Allan, J. D. Landscapes and riverscapes: The influence of land use on stream ecosystems. Annu. Rev. Ecol. Evol. Syst. 35, 257–284. https://doi.org/10.1146/annurev.ecolsys.35.120202.110122 (2004).Article 

    Google Scholar 
    Paul, M. J. & Meyer, J. L. Streams in the urban landscape. Annu. Rev. Ecol. Evol. Syst. 32, 333–365. https://doi.org/10.1146/annurev.ecolsys.32.081501.114040 (2001).Article 

    Google Scholar 
    Wicks, C., Kelley, C. & Peterson, E. Estrogen in a karstic aquifer. Groundwater 42, 384–389. https://doi.org/10.1111/j.1745-6584.2004.tb02686.x (2004).Article 

    Google Scholar 
    Buřič, M., Kouba, A., Máchová, J., Mahovská, I. & Kozák, P. Toxicity of the organophosphate pesticide diazinon to crayfish of differing age. Int. J. Environ. Sci. Technol. 10, 607–610. https://doi.org/10.1007/s13762-013-0185-4 (2013).Article 

    Google Scholar 
    Sohn, L., Brodie, R. J., Couldwell, G., Demmons, E. & Sturve, J. Exposure to a nicotinoid pesticide reduces defensive behaviors in a non-target organism, the rusty crayfish Orconectes rusticus. Ecotoxicology 27, 900–907. https://doi.org/10.1007/s10646-018-1950-4 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Noltie, D. B. & Wicks, C. M. How hydrogeology has shaped the ecology of Missouri’s Ozark cavefish, Amblyopsis rosae, and southern cavefish, Typhlichthys subterraneus: Insights on the sightless from understanding the underground. Environ. Biol. Fish. 62, 171–194. https://doi.org/10.1023/A:1011815806589 (2001).Article 

    Google Scholar 
    Kuhajda, B. R. & Mayden, R. L. Status of the federally endangered Alabama cavefish, Speoplatyrhinus poulsoni (Amblyopsidae), in Key Cave and surrounding caves, Alabama. Environ. Biol. Fish. 62, 215–222. https://doi.org/10.1023/A:1011817023749 (2001).Article 

    Google Scholar 
    Hutchins, B. T. The conservation status of Texas groundwater invertebrates. Biodivers. Conserv. 27, 475–501. https://doi.org/10.1007/s10531-017-1447-0 (2018).Article 

    Google Scholar 
    Niemiller, M. L. et al. Discovery of a new population of the federally endangered Alabama cave shrimp, Palaemonias alabamae Smalley, 1961, in northern Alabama. Subterr. Biol. 32, 43–59. https://doi.org/10.3897/subtbiol.32.38280 (2019).Article 

    Google Scholar 
    Abell, R., Allan, J. D. & Lehner, B. Unlocking the potential of protected areas for freshwaters. Biol. Conserv. 134, 48–63. https://doi.org/10.1016/j.biocon.2006.08.017 (2007).Article 

    Google Scholar 
    Liu, Y. et al. A review on effectiveness of best management practices in improving hydrology and water quality: Needs and opportunities. Sci. Total Environ. 601–602, 580–593. https://doi.org/10.1016/j.scitotenv.2017.05.212 (2017).Article 
    ADS 
    PubMed 

    Google Scholar  More