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    Transmission of stony coral tissue loss disease (SCTLD) in simulated ballast water confirms the potential for ship-born spread

    Precht, W. F., Gintert, B. E., Robbart, M. L., Fura, R. & van Woesik, R. Unprecedented disease-related coral mortality in Southeastern Florida. Sci. Rep. 6, 31374 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    NOAA. Stony Coral Tissue Loss Disease Case Definition. NOAA, Silver Spring, MD 10 (2018).Aeby, G. S. et al. Pathogenesis of a tissue loss disease affecting multiple species of corals along the Florida Reef Tract. Front Mar. Sci. 6, 00678 (2019).
    Google Scholar 
    Landsberg, J. H. et al. Stony coral tissue loss disease in Florida is associated with disruption of host–zooxanthellae physiology. Front Mar. Sci. 7, 576013 (2020).
    Google Scholar 
    Neely, K. L., Macaulay, K. A., Hower, E. K. & Dobler, M. A. Effectiveness of topical antibiotics in treating corals affected by Stony Coral Tissue Loss Disease. PeerJ 8, 9289 (2020).
    Google Scholar 
    Shilling, E. N., Combs, I. R. & Voss, J. D. Assessing the effectiveness of two intervention methods for stony coral tissue loss disease on Montastraea cavernosa. Sci. Rep. 11, 8566 (2021).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Walker, B. K., Turner, N. R., Noren, H. K. G., Buckley, S. F. & Pitts, K. A. Optimizing stony coral tissue loss disease (SCTLD) intervention treatments on Montastraea cavernosa in an endemic zone. Front Mar. Sci. 8, 666224 (2021).
    Google Scholar 
    Work, T. M. et al. Viral-like particles are associated with endosymbiont pathology in Florida corals affected by stony coral tissue loss disease. Front Mar. Sci. 8, 750658 (2021).
    Google Scholar 
    Veglia, A. J. et al. Alphaflexivirus genomes in stony coral tissue loss disease-affected, disease-exposed, and disease-unexposed coral colonies in the U.S. Virgin Islands. Microbiol. Resource Announc. 11, e01199-e1221 (2022).CAS 

    Google Scholar 
    Rosales, S. M. et al. Bacterial metabolic potential and micro-eukaryotes enriched in stony coral tissue loss disease lesions. Front Mar. Sci. 8, 776859 (2022).
    Google Scholar 
    Rosales, S. M., Clark, A. S., Huebner, L. K., Ruzicka, R. R. & Muller, E. M. Rhodobacterales and Rhizobiales are associated with stony coral tissue loss disease and its suspected sources of transmission. Front. Microbiol. 11, 681 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    Studivan, M. S. et al. Reef sediments can act as a stony coral tissue loss disease vector. Front Mar. Sci. 8, 815698 (2022).
    Google Scholar 
    Meyer, J. L. et al. Microbial community shifts associated with the ongoing stony coral tissue loss disease outbreak on the Florida Reef Tract. Front. Microbiol. 10, 2244 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    Ushijima, B. et al. Disease diagnostics and potential coinfections by Vibrio coralliilyticus during an ongoing coral disease outbreak in Florida. Front. Microbiol. 11, 2682 (2020).
    Google Scholar 
    Meiling, S. S. et al. Variable species responses to experimental stony coral tissue loss disease (SCTLD) exposure. Front Mar. Sci. 8, 670829 (2021).
    Google Scholar 
    Becker, C. C., Brandt, M., Miller, C. A. & Apprill, A. Microbial bioindicators of stony coral tissue loss disease identified in corals and overlying waters using a rapid field-based sequencing approach. Environ. Microbiol. 24, 1166–1182 (2021).PubMed 

    Google Scholar 
    Dobbelaere, T., Muller, E. M., Gramer, L. J., Holstein, D. M. & Hanert, E. Coupled epidemio-hydrodynamic modeling to understand the spread of a deadly coral disease in Florida. Front Mar. Sci. 7, 591881 (2020).
    Google Scholar 
    Dobbelaere, T. et al. Connecting the dots: Transmission of stony coral tissue loss disease from the Marquesas to the Dry Tortugas. Front Mar. Sci. 9, 778938 (2022).
    Google Scholar 
    Muller, E. M., Sartor, C., Alcaraz, N. I. & van Woesik, R. Spatial epidemiology of the stony-coral-tissue-loss disease in Florida. Front Mar. Sci. 7, 00163 (2020).
    Google Scholar 
    Sharp, W. C., Shea, C. P., Maxwell, K. E., Muller, E. M. & Hunt, J. H. Evaluating the small-scale epidemiology of the stony-coral-tissue-loss-disease in the middle Florida Keys. PLoS ONE 15, e0241871 (2020).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Williamson, O. M., Dennison, C. E., O’Neil, K. L. & Baker, A. C. Susceptibility of Caribbean brain coral recruits to stony coral tissue loss disease (SCTLD). Front Mar. Sci. 9, 821165 (2022).
    Google Scholar 
    Noonan, K. R. & Childress, M. J. Association of butterflyfishes and stony coral tissue loss disease in the Florida Keys. Coral Reefs 39, 1581–1590 (2020).
    Google Scholar 
    Dahlgren, C., Pizarro, V., Sherman, K., Greene, W. & Oliver, J. Spatial and temporal patterns of stony coral tissue loss disease outbreaks in the Bahamas. Front Mar. Sci. 8, 682114 (2021).
    Google Scholar 
    Rosenau, N. A. et al. Considering commercial vessels as potential vectors of stony coral tissue loss disease. Front Mar. Sci. 8, 709764 (2021).
    Google Scholar 
    Roth, L., Kramer, P., Doyle, E. & O’Sullivan, C. Caribbean SCTLD Dashboard. Available www.agrra.org. Accessed 06 Mar 2021. (2020).Brandt, M. E. et al. The emergence and initial impact of stony coral tissue loss disease (SCTLD) in the United States Virgin Islands. Front Mar. Sci. 8, 715329 (2021).
    Google Scholar 
    Bailey, S. A. et al. Trends in the detection of aquatic non-indigenous species across global marine, estuarine and freshwater ecosystems: A 50-year perspective. Divers. Distrib. 26, 1780–1797 (2020).MathSciNet 

    Google Scholar 
    Hewitt, C. L., Gollasch, S. & Minchin, D. The vessel as a vector: Biofouling, ballast water and sediments. In Biological Invasions in Marine Ecosystems Vol. 204 (eds Rilov, G. & Crooks, J. A.) 117–131 (Springer, 2009).
    Google Scholar 
    Zabin, C. J. et al. Small boats provide connectivity for nonindigenous marine species between a highly invaded international port and nearby coastal harbors. Manag. Biol. Invas. 5, 97–112 (2014).
    Google Scholar 
    Ashton, G. V., Zabin, C. J., Davidson, I. C. & Ruiz, G. M. Recreational boats routinely transfer organisms and promote marine bioinvasions. Biol. Invas. 24, 1083–1096 (2022).
    Google Scholar 
    Drake, L. A., Doblin, M. A. & Dobbs, F. C. Potential microbial bioinvasions via ships’ ballast water, sediment, and biofilm. Mar. Pollut. Bull. 55, 333–341 (2007).CAS 
    PubMed 

    Google Scholar 
    Pagenkopp Lohan, K. M., Fleischer, R. C., Carney, K. J., Holzer, K. K. & Ruiz, G. M. Amplicon-based pyrosequencing reveals high diversity of protistan parasites in ships’ ballast water: Implications for biogeography and infectious diseases. Microb. Ecol. 71, 530–542 (2015).PubMed 

    Google Scholar 
    Ruiz, G. M. et al. Global spread of microorganisms by ships. Nature 408, 49–50 (2000).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Hwang, J., Park, S. Y., Lee, S. & Lee, T. K. High diversity and potential translocation of DNA viruses in ballast water. Mar. Pollut. Bull. 137, 449–455 (2018).CAS 
    PubMed 

    Google Scholar 
    Shikuma, N. J. & Hadfield, M. G. Marine biofilms on submerged surfaces are a reservoir for Escherichia coli and Vibrio cholerae. Biofouling 26, 39–46 (2009).
    Google Scholar 
    Aguirre-Macedo, M. L. et al. Ballast water as a vector of coral pathogens in the Gulf of Mexico: The case of the Cayo Arcas coral reef. Mar. Pollut. Bull. 56, 1570–1577 (2008).CAS 
    PubMed 

    Google Scholar 
    Bruno, J. F. The coral disease triangle. Nat. Clim. Chang. 5, 302–303 (2015).ADS 

    Google Scholar 
    Lakshmi, E., Priya, M. & Achari, V. S. An overview on the treatment of ballast water in ships. Ocean Coast. Manag. 199, 105296 (2021).
    Google Scholar 
    Petersen, N. B., Madsen, T., Glaring, M. A., Dobbs, F. C. & Jørgensen, N. O. G. Ballast water treatment and bacteria: Analysis of bacterial activity and diversity after treatment of simulated ballast water by electrochlorination and UV exposure. Sci. Total Environ. 648, 408–421 (2019).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Romero-Martínez, L., Moreno-Andrés, J., Acevedo-Merino, A. & Nebot, E. Evaluation of ultraviolet disinfection of microalgae by growth modeling: Application to ballast water treatment. J. Appl. Phycol. 28, 2831–2842 (2016).
    Google Scholar 
    First, M. R. et al. Stratification of living organisms in ballast tanks: How do organism concentrations vary as ballast water is discharged?. Environ. Sci. Technol. 47, 4442–4448 (2013).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Drake, L. A. et al. Microbial ecology of ballast water during a transoceanic voyage and the effects of open-ocean exchange. Mar. Ecol. Prog. Ser. 233, 13–20 (2002).ADS 

    Google Scholar 
    Khandeparker, L., Kuchi, N., Desai, D. V. & Anil, A. C. Changes in the ballast water tank bacterial community during a trans-sea voyage: Elucidation through next generation DNA sequencing. J. Environ. Manag. 273, 111018 (2020).
    Google Scholar 
    Ruiz, G. M., Lorda, J., Arnwine, A. & Lion, K. Shipping patterns associated with the Panama Canal: Effects on biotic exchange? In Bridging Divides Vol. 83 (eds Gollasch, S. et al.) 113–126 (Springer, 2006).
    Google Scholar 
    Pagano, A., Wang, G., Sánchez, O., Ungo, R. & Tapiero, E. The impact of the Panama Canal expansion on Panama’s maritime cluster. Marit. Policy Manag. 43, 164–178 (2016).
    Google Scholar 
    Muirhead, J. R., Minton, M. S., Miller, W. A. & Ruiz, G. M. Projected effects of the Panama Canal expansion on shipping traffic and biological invasions. Divers. Distrib. 21, 75–87 (2015).
    Google Scholar 
    Ros, M. et al. The Panama Canal and the transoceanic dispersal of marine invertebrates: Evaluation of the introduced amphipod Paracaprella pusilla Mayer, 1890 in the Pacific Ocean. Mar. Environ. Res. 99, 204–211 (2014).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Stehouwer, P. P., Buma, A. & Peperzak, L. A comparison of six different ballast water treatment systems based on UV radiation, electrochlorination and chlorine dioxide. Environ. Technol. 36, 2094–2104 (2015).CAS 
    PubMed 

    Google Scholar 
    Wu, Y., Li, Z., Du, W. & Gao, K. Physiological response of marine centric diatoms to ultraviolet radiation, with special reference to cell size. J. Photochem. Photobiol., B 153, 1–6 (2015).CAS 

    Google Scholar 
    Aguirre, L. E. et al. Diatom frustules protect DNA from ultraviolet light. Sci. Rep. 8, 5138 (2018).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    First, M. R. & Drake, L. A. Life after treatment: Detecting living microorganisms following exposure to UV light and chlorine dioxide. J. Appl. Phycol. 26, 227–235 (2014).CAS 

    Google Scholar 
    Liebich, V., Stehouwer, P. P. & Veldhuis, M. Re-growth of potential invasive phytoplankton following UV-based ballast water treatment. Aquat. Invas. 7, 29–36 (2012).
    Google Scholar 
    Hess-Erga, O. K., Moreno-Andrés, J., Enger, Ø. & Vadstein, O. Microorganisms in ballast water: Disinfection, community dynamics, and implications for management. Sci. Total Environ. 657, 704–716 (2019).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Endresen, Ø., Lee Behrens, H., Brynestad, S., Bjørn Andersen, A. & Skjong, R. Challenges in global ballast water management. Mar. Pollut. Bull. 48, 615–623 (2004).CAS 
    PubMed 

    Google Scholar 
    Vorkapić, A., Radonja, R. & Zec, D. Cost efficiency of ballast water treatment systems based on ultraviolet irradiation and electrochlorination. Promet Traffic Transp. 30, 343–348 (2018).
    Google Scholar 
    King, D., Hagan, P., Riggio, M. & Wright, D. Preview of global ballast water treatment markets. J. Mar. Eng. Technol. 11, 3–15 (2012).
    Google Scholar 
    Wang, Z., Saebi, M., Corbett, J. J., Grey, E. K. & Curasi, S. R. Integrated biological risk and cost model analysis supports a geopolitical shift in ballast water management. Environ. Sci. Technol. 55, 12791–12800 (2021).CAS 
    PubMed 

    Google Scholar 
    Moreno-Andrés, J. & Peperzak, L. Operational and environmental factors affecting disinfection byproducts formation in ballast water treatment systems. Chemosphere 232, 496–505 (2019).ADS 
    PubMed 

    Google Scholar 
    David, M., Linders, J., Gollasch, S. & David, J. Is the aquatic environment sufficiently protected from chemicals discharged with treated ballast water from vessels worldwide? A decadal environmental perspective and risk assessment. Chemosphere 207, 590–600 (2018).ADS 
    CAS 
    PubMed 

    Google Scholar 
    U.S. Environmental Protection Agency. Generic protocol for the verification of ballast water treatment technology, version 5.1. Report number EPA/600/R-10/146. Washington, D.C. 157 (2010).Evans, J. S., Paul, V. J., Ushijima, B. & Kellogg, C. A. Combining tangential flow filtration and size fractionation of mesocosm water as a method for the investigation of waterborne coral diseases. Biol. Methods Protocols 7, bpac007 (2022).
    Google Scholar 
    Fujimoto, M. et al. Application of Ion Torrent sequencing to the assessment of the effect of alkali ballast water treatment on microbial community diversity. PLoS ONE 9, e107534 (2014).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    United States Coast Guard. Ballast Water Best Management Practices to Reduce the Likelihood of Transporting Pathogens That May Spread Stony Coral Tissue Loss Disease. Marine Safety Information Bulletin 07–19. Washington, D.C. 2 (2019).Bolton, J. R. & Linden, K. G. Standardization of methods for fluence (UV dose) determination in bench-scale UV experiments. J. Environ. Eng. 129, 209–215 (2003).CAS 

    Google Scholar 
    Enochs, I. C. et al. The influence of diel carbonate chemistry fluctuations on the calcification rate of Acropora cervicornis under present day and future acidification conditions. J. Exp. Mar. Biol. Ecol. 506, 135–143 (2018).CAS 

    Google Scholar 
    R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/. Preprint at https://www.r-project.org/ (2019).Therneau, T. M. survival: A package for survival analysis in R. R package version 3.2–13. (2021).Kassambara, A., Kosinski, M. & Biecek, P. survminer: Drawing survival curves using “ggplot2”. R package version 0.4.9. (2021).Bakalar, G. Review of interdisciplinary devices for detecting the quality of ship ballast water. Springerplus 3, 468 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    Water Environmental Federation & American Public Health Association. Standard methods for the examination of water and wastewater. Washington, D.C. 21 (2005).Steinberg, M. K., Lemieux, E. J. & Drake, L. A. Determining the viability of marine protists using a combination of vital, fluorescent stains. Mar. Biol. 158, 1431–1437 (2011).
    Google Scholar 
    Oksanen, J. et al. vegan: Community ecology package. R package version 2.0–10. (2015).Martinez Arbizu, P. pairwiseAdonis: Pairwise multilevel comparison using adonis. R package version 0.4. (2020).Studivan, MS. Mstudiva/SCTLD-ballast-transmission: Stony coral tissue loss disease ballast transmission and treatment (Version 1.0), Zenodo, https://doi.org/10.5281/zenodo.6561517 (2022). More

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    African perspectives on climate change research

    Urbanization is fast progressing in the Global South, requiring new solutions for infrastructure, services, industrial development and land and energy use for these regions. In this context, fast-growing cities in Africa can take on a leadership role in driving climate change mitigation and adaptation, disaster risk reduction and sustainable development.
    Credit: Stefan Rotter / Alamy Stock PhotoCities in Africa and elsewhere in the Global South continue to grapple with the challenge of delivering equitable services, infrastructure, housing and action to respond to climate change extremes and disasters. One well-known problem is a mismatch between the pace of urban growth and the slower development of basic services and critical infrastructure. This results in, for example, deficient sanitation, water supply systems and localized waste management for large parts of the population, which in turn contribute substantially to heightened poverty and inequality. For inclusive, equitable, prosperous and climate-resilient cities, urban management needs to integrate low-income communities into the urban economy by ensuring access to water, sanitation, energy transition, waste management, poverty reduction and by improving resilience through innovative solutions.
    Credit: Patrick J. Endres/Corbis Documentary/GettySuch an equitable urban transition requires changes in the urban infrastructure, and land and energy use, as well as water and ecosystem management. The key research question in this field is to find ways to ensure city-wide access to infrastructure and services, while minimizing emissions and resource use, and building resilience to climate change impacts. In this regard, cities in the Global South and Africa in particular can serve as examples for other parts of the world as they have the potential to adopt disruptive, innovative yet practical solutions to low emissions, resource minimization and resilience building.
    Credit: Nature Picture Library / Alamy Stock PhotoFor example, rapid urbanization creates the opportunity to develop economic structures in African cities that strongly integrate waste by promoting recovery, recycling, re-use and repair for lengthening lifecycles. Such a circular economy can create business opportunities, while also reducing resource use, thus creating a pathway for sustainable development. Another potential solution is hybrid systems for urban water management that are off-grid and utilize multiple water sources and treatment but that can also connect to centralized water systems. Business models for micro-to-medium enterprises have the potential to integrate some of the low-income groups through these kinds of technology and building social resilience.
    Credit: Images of Africa Photobank / Alamy Stock PhotoThese examples are part of a broader assessment of urban infrastructure innovations, their disruption of centralized systems and rethinking of urban form for more compact, walkable, co-located land use for low carbon intensity towards net-zero cities. However, to translate research on these new solutions into action, a shift is necessary in the planning, governing and managing of cities so as to allow for opportunities for leapfrogging to emerge and expand the possibilities of urban development for inclusive and resilient African cities. More

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    Assessing data bias in visual surveys from a cetacean monitoring programme

    Data processingIn 2019, the CETUS data spanning between 2012 and 2017 was published open access through the Flanders Marine Institute (VLIZ) IPT portal and distributed by EMODnet and OBIS, in a first version of the CETUS dataset9. The data collected between 2018 and 2019 was prepared as the 2012–2017 data9. Methods for photographic verification/validation and to evaluate the MMOs experience were applied (see below), in order to include new variables on data quality in an updated version of the dataset. Currently, the CETUS dataset is updated, with a 2nd version available10. It comprises data from 2012 to 2017, with the following two new columns on the observers’ experience: “most experienced observer” and “least experienced observer”; and a new column associated with validation of the sightings’ identifications: “photographic validation”. The results here presented correspond to the analysis of the data from 2012 to 2019, and the open-access dataset will soon be further updated with the 2018–2019 data.Photographic verificationAll the former MMOs who have integrated the CETUS Project, between 2012 and 2019, were contacted and asked to provide any available photographic or video records of cetaceans collected during their on board periods. The collection of sighting’s images was not a requirement of the CETUS protocol, and so these records were obtained opportunistically, with availability and quality depending on several factors: observers on board having personal cameras, camera quality, intention of the observer taking the photograph (e.g., for aesthetic or identification purposes).The images obtained were organized in a folder hierarchy from the year to the day of recording. However, not all the images had metadata up to the day of recording, so these were inserted into the most appropriate hierarchy-level of the folder organization. For each set of records corresponding to a single-taxon sighting, the photos/videos with the better quality or framing (i.e., that allowed for an easier species identification) were selected for that sighting. The remaining photos/videos were only consulted in case of doubt (e.g., to look for additional details that could help with the identification).Verification consisted of the process of matching the photographic/video records with the dataset sighting registers. Whenever possible and ideally, the file metadata was used for the process. However, often, the date and/or time of the file metadata were wrong, non-existent, or in different time zones. In these cases, a conservative methodology was applied using all available information to match as many sightings as possible. An estimation of time lag was attempted (based on, at least, two obvious matches between photographs/videos and dataset registers, e.g., unique sighting of the day, close to the boat, easy/obvious identification). When not possible, further evaluation consisted in assessing whether the sighting and image record was too obvious, and accounting for unique complementary information on the sighting (e.g., the number of animals or the side of the sighting were unique for that day and/or for that species/group).Photographic validationAfter the verification process, the validation of the matched records was carried out, to confirm or correct the species identification of sightings in the 1st version of the CETUS dataset (i.e., reported by the MMOs on board). The validation approach involved, for more dubious identification through the photo/video records, the discussion between four experienced observers of the CETUS team. In cases where no consensual agreement was achieved, an external expert on cetacean identification was also consulted. Identifications made through the photographic/video records required 100% certainty, and these were then compared with the cetacean identifications provided in the 1st version of the CETUS dataset. Then, the occurrence records with originally misidentifications of cetaceans, as well as those records where validation allowed to achieve an identification to a lower taxon, were corrected in the 2nd version of the dataset (i.e., a delphinid sighting validated as common dolphin, will now appear as common dolphin). A new column “photographic validation” was added to the dataset with the following categories: “yes” (i.e., validated with photograph/video), “no” (i.e., not validated with photograph/video), and “to the family” (i.e., validation only to the family taxon).For further analysis, specifically for the model process on the identification success (see below), registers were considered “completely validated” if it was possible to complete the photographic/video identification process up to the species level (then, differentiating if the original identification from the MMOs was or not correct). For Globicephala sp. and Kogia sp., validation to the genus was considered complete, since the species from both genera are visually hardly differentiated, especially at sea.Creating a data quality criteria: evaluating MMOs experienceQuality criteria were created to evaluate the MMOs experience based on the information collected from their curricula vitae (CVs) (alumni MMOs provided as many CVs as the years of their participation in CETUS). The following quality criteria were considered: (i) the experience at sea, (ii) the experience with cetaceans’ ID, (iii) the number of species they have worked with, and (iv) the experience working with the CETUS Project protocol. Each of these quality criteria was ranked from 0 to 5, and then these were summed to generate an evaluation score, on a scale of 0 to 20, attributed to each MMO (Table 4).Table 4 Quality criteria for MMOs evaluation.Full size tableThe MMOs evaluations were computed for each cruise (i.e., the trip from one port to another), considering the experience of the MMOs based on the CV obtained for that year, plus the experience acquired during CETUS participation in previous cruises that year. Since most of the times, the team of observers on board each cruise was constituted by two MMOs, two final evaluation scores were attributed to each cruise in the 2nd version of the CETUS dataset, into two new columns: “most experienced observer” and “least experienced observer”. On rare occasions where there is only one observer on board that cruise, only the evaluation of the single observer was included under the column “most experienced observer”, leaving the column “least experienced observer” as “NULL”. To investigate the experience of MMOs on board, both individually and cumulative (LEO + MEO), the combination of the score values was computed by cruise. These were then trimmed to unique combinations of evaluation scores.The names of observers, previously presented in the online dataset for each cruise, were removed for anonymity purposes, as there is now ancillary information regarding their experience.Model fittingTwo Generalized Additive Models (GAM) were fitted to assess bias on the number of sightings recorded per survey and on the identification success of cetacean species. Details for each model are presented below. Both models were fitted in R (Version 4.1.0). Prior to modelling, Pearson correlations were calculated between all pairs of explanatory variables, considered for each model (see below), to exclude highly correlated variables, considering a threshold of 0.7524,25,28. Since the variables regarding MMOs’ experience were correlated (LEO or MEO correlated with cumulative and mean experience; and cumulative experience correlated with mean experience – Supplementary Fig. S3), these variables were not included in the first fitting stage (backward selection) but included later through forward selection (see below). Multicollinearity among explanatory variables was measured through the Variance Inflation Factor (VIF), with a threshold of 3 (Supplementary Tables S4)24,25,29. After removing the MMOs evaluation scores, no multicollinearity was observed, so all the other variables were kept for the first fitting stage.For model selection, a backward selection was applied to oversaturated models18,24,25,30,31. The Akaike Information Criterion (AIC) was used as a measure of adequation of fitness, choosing the model with the lowest AIC value at each step of the model fitting process, i.e., comparing nested models (larger model incorporating one more explanatory variable compared with the smaller model). If the AIC-difference between the two models was less than 2, an Analysis of Variance (ANOVA), through chi-square test, was used to check if the AIC-difference was significant24,25,32. If this difference was not statistically significant (p  > 0.05), the simplest model (smaller model) was kept. Through a forward selection process, the variables regarding the MMOs evaluation scores were added, one at a time, to the best model obtained in the previous backward selection. After comparing the models with each other (separate variables for LEO + MEO vs. Cumulative Evaluation vs Mean Evaluation), the best model, considering the AIC value, was kept. A final backward selection process was then applied.All GAMs were fitted with the “mgcv” package (https://cran.r-project.org/web/packages/mgcv) and a maximum of four splines (k = 4) was chosen to limit the complexity of smoothers describing the effects of the explanatory variables25,31. If a spline was close to linear (with estimated degrees of freedom of ~1), the smooth term was removed, and a linear function was fitted. To check for model quality, the “gam.check” function was used to verify the diagnostic plots and the adequacy of the number of splines (Supplementary Figs. S5 and S6). Existence of influential data points was assessed (with the threshold of 0.25 for the Hat values), as well as the correlation between model residuals and explanatory variables. In both final models, number of splines was adequate and there were no influential data points or clear correlation between residuals and explanatory variables (Supplementary Figs. S7 and S8)24,32.Bias modelling of number of sightingsTo assess the bias parameters on the number of sightings recorded per survey (i.e., a full day monitoring, from sunrise to sunset), the following detectability factors were considered as explanatory variables: weather conditions (i.e., the minimums and maximums of the sea state, wind state, and visibility), the experience of MMOs (i.e., the evaluation scores of the least and the most experienced observers, as well as the mean and cumulative evaluations of the MMOs experience) and kilometres sampled “on-effort” (i.e., periods of active survey). Sampling periods were divided into “On-effort” and “Off-effort” conditions, based on four meteorological variables: sea state (Douglas scale), wind state (Beaufort scale), visibility (measured in a categorical scale ranging from 0–10 and estimated from the distance to the horizon line and possible reference points at a known range, e.g., ships with an automatic identification system,  > 1000 km), and the occurrence of rain (see Supplementary Table S9)10. For the model fitting, only “on-effort” periods of sampling were considered. Given that the response variable was count data, a Poisson distribution was tested (with a log link function). Then, the resulting first oversaturated model was checked for overdispersion, through a Pearson estimator. Since it tested positive for overdispersion (φ = 1.99), a negative binomial distribution (with a log link function) was fitted.Bias modelling of identification successA binary response variable, based on the success in the species identification for each sighting, was generated, and a model with binomial distribution (with a logit link function) was fitted. As in the previous model, only “on-effort” records were used. The total number of non-successful identifications across the dataset (the 0 s of the model) was extrapolated from the proportion of wrong identifications obtained in the validation process. To calculate this proportion, only complete validated sightings registered “on-effort” were used. Proportions were computed and extrapolated to Odontoceti and Mysticeti, separately. This resulted in 78 non-successful identifications in delphinids, plus 17 misidentifications in baleen whales, i.e., a total of 95 “on-effort” sightings randomly selected from the dataset were defined as unsuccessful identifications (0 s in the response variable for model fitting). The remaining records were considered successful identifications (1 s in the response variable for model fitting). To assess the bias parameters on the identification success, the following independent variables were considered in the analysis: the group (i.e., Group A: Odontoceti sightings, excluding sperm whale (Physeter macrocephalus); and Group B: Mysticeti sightings, plus sperm whale), the size of the group (i.e., the best estimate of the number of animals in a sighting, from the observer’s perspective), sighting distance (i.e., a relative measure according to the scale of the binoculars), weather conditions (i.e., the sea state, wind state, and visibility at the time of each sighting), the experience of MMOs (i.e., the evaluation scores of least and most experienced observers, as well as the mean and cumulative scores of the MMOs teams). Group A and B were settled according to cetacean morphology. However, since sperm whales have closer similarities with Mysticeti species, they were also included in Group B21,33. This categorization was mostly based on body size, as this is likely the main factor, regarding the species morphology, influencing the identification. Group A is constituted by species with a medium length of less than 10 meters, while Group B includes the larger species over 10 meters (Mysticeti plus P. macrocephalus)33. Since in the CETUS Project, different binoculars have been used – with two different reticle scales – it was necessary to standardize binocular distances to the same scale. More

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    Microbiome diversity and metabolic capacity determines the trophic ecology of the holobiont in Caribbean sponges

    Gardner TA, Cote IM, Gill JA, Grant A, Watkinson AR. Long-term region-wide declines in Caribbean corals. Science. 2003;301:958–60.CAS 
    PubMed 

    Google Scholar 
    Knowlton N. The future of coral reefs. Proc Natl Acad Sci USA. 2001;98:5419–25.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Worm B, Barbier EB, Beaumont N, Duffy JE, Folke C, Halpern BS, et al. Impacts of biodiversity loss on ocean ecosystem services. Science. 2006;314:787–90.CAS 
    PubMed 

    Google Scholar 
    Dudgeon SR, Aronson RB, Bruno JF, Precht WF. Phase shifts and stable states on coral reefs. Mar Ecol Prog Ser. 2010;413:201–16.
    Google Scholar 
    Bell JJ, Davy SK, Jones T, Taylor MW, Webster NS. Could some coral reefs become sponge reefs as our climate changes? Glob Climate Change. 2013;19:2613–24.
    Google Scholar 
    McMurray SE, Henkel TP, Pawlik JR. Demographics of increasing populations of the giant barrel sponge Xestospongia muta in the Florida Keys. Ecology. 2010;91:560–70.PubMed 

    Google Scholar 
    Bell JJ. The functional roles of marine sponges. Est Coast Shelf Sci. 2008;79:341–53.
    Google Scholar 
    Lesser MP, Slattery M. Will coral reef sponges be winners in the Anthropocene? Glob Change Biol. 2020;26:3202–11.
    Google Scholar 
    Pankey MS, Plachetzki DC, Macartney KJ, Gastaldi M, Slattery M, Gochfeld DJ, et al. Co-phylogeny and convergence shape holobiont evolution in sponge-microbe symbioses. Nat Ecol Evol. 2022;6:750–62.
    Google Scholar 
    Lesser MP, Slattery M, Mobley CD. Biodiversity and functional ecology of mesophotic coral reefs. Ann Rev Ecol Syst. 2018;49:49–71.
    Google Scholar 
    Diaz MC, Rützler K. Sponges: an essential component of Caribbean coral reefs. Bull Mar Sci. 2001;69:535–46.
    Google Scholar 
    Wulff JL. Ecological interactions and the distribution, abundance, and diversity of sponges. Adv Mar Biol. 2012;61:273–344.PubMed 

    Google Scholar 
    Lesser MP. Benthic-pelagic coupling on coral reefs: feeding and growth of Caribbean sponges. J Exp Mar Biol Ecol. 2006;328:277–88.
    Google Scholar 
    Perea-Blazquez A, Davy SK, Bell JJ. Estimates of particulate organic carbon flowing from the pelagic environment to the benthos through sponge assemblages. PLoS One. 2012;7:e29569.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Lesser MP, Slattery M. Ecology of Caribbean sponges: are top-down or bottom-up processes more important? PLoS One. 2013;8:e79799.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Pawlik JR. The chemical ecology of sponges on Caribbean reefs: natural products shape natural systems. BioScience. 2011;61:888–98.
    Google Scholar 
    Slattery M, Gochfeld DJ. Chemical interactions among marine competitors, and host-pathogens. In: Fattorusso, E, Gerwick, WH, Taglialatela-Scafati, O (eds). Handbook of Marine Natural Products. Springer, 2012. pp. 824–59.Thacker RW, Freeman CJ. Sponge-microbe symbioses: recent advances and new directions. Adv Mar Biol. 2012;62:57–112.PubMed 

    Google Scholar 
    Taylor MW, Radax R, Steger D, Wagner M. Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Biol Rev. 2007;71:295–347.CAS 

    Google Scholar 
    Schmitt S, Tsai P, Bell J, Fromont J, Ilan M, Lindquist N, et al. Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME J. 2012;6:564–76.CAS 
    PubMed 

    Google Scholar 
    Gloeckner V, Wehrl M, Moitinho-Silva L, Gernert C, Schupp P, Pawlik JR, et al. The HMA-LMA dichotomy revisited: an electron microscopical survey of 56 sponge species. Biol Bull. 2014;227:78–88.PubMed 

    Google Scholar 
    Hentschel U, Fieseler L, Wehrl M, Gernert C, Steinert M, Hacker J, et al. Microbial diversity of marine sponges. Prog Mol Subcell Biol. 2003;37:59–88.CAS 
    PubMed 

    Google Scholar 
    Fiore CL, Jarett JK, Olson ND, Lesser MP. Nitrogen fixation and nitrogen transformation in marine symbioses. Trends Microbiol. 2010;18:455–63.CAS 
    PubMed 

    Google Scholar 
    Zhang F, Jonas L, Lin H, Hill RT. Microbially mediated nutrient cycles in marine sponges. FEMS Microbiol Ecol. 2019;95:115.
    Google Scholar 
    Schläppy M-L, Schöttner SI, Lavik G, Kuypers MMM, de Beer D, Hoffmann F. Evidence of nitrification and denitrification in high and low microbial abundance sponges. Mar Biol. 2010;157:593–602.PubMed 

    Google Scholar 
    Giles EC, Kamke J, Moitinho-Silva L, Taylor MW, Hentschel U, Ravasi T, et al. Bacterial community profiles in low microbial abundance sponges. FEMS Microbiol Ecol. 2013;83:232–41.CAS 
    PubMed 

    Google Scholar 
    Weisz JB, Lindquist N, Martens CS. Do associated microbial abundances impact marine demosponge pumping rates and tissue densities. Oecologia. 2008;155:367–76.PubMed 

    Google Scholar 
    de Goeij JM, van Oevelen D, Vermiej MJA, Osinga R, Middelburg JJ, de Goeij AFPM, et al. Surviving in a marine desert: the sponge loop retains resources within coral reefs. Science. 2013;342:108–10.PubMed 

    Google Scholar 
    de Goeij JM, Lesser MP, Pawlik JR. Nutrient fluxes and ecological functions of coral reef sponges in a changing ocean. In: Carballo, J, Bell, J eds. Climate Change, Ocean Acidification and Sponges. Springer, 2017. pp 373–410.Tanaka Y, Miyajima T, Wtanabe A, Nadaoka K, Yamamoto T, Ogawa H. Distribution of dissolved organic carbon and nitrogen in a coral reef. Coral Reefs. 2011;30:533–41.
    Google Scholar 
    Lesser MP, Slattery M, Laverick JH, Macartney KJ, Bridge TC. Global community breaks at 61 m on mesophotic coral reefs. Global Ecol Biogeogr. 2019;28:1403–16.
    Google Scholar 
    Lønborg C, Álvarez-Salgado XA, Duggan S, Carreira C. Organic matter bioavailability in tropical coastal waters: The Great Barrier Reef. Limnol Oceanogr. 2018;63:1015–35.
    Google Scholar 
    Macartney KJ, Abraham AC, Slattery M, Lesser MP. Growth and feeding in the sponge Agelas tubulata from shallow to mesophotic depths on Grand Cayman Island. Ecosphere. 2021;12:e03764.
    Google Scholar 
    Ribes M, Coma R, Atkinson MJ, Kinzie RA. Particle removal by coral reef communities: picoplankton is a major source of nitrogen. Mar Ecol Prog Ser. 2003;257:13–23.
    Google Scholar 
    Ribes M, Coma R, Atkinson MJ, Kinzie RA. Sponges and ascidians control removal of particulate organic nitrogen from coral reef water. Limnol Oceanogr. 2005;50:1480–9.CAS 

    Google Scholar 
    Maldonado M, Ribes M, van Duyl FC. Nutrient fluxes through sponges: biology, budgets, and ecological implications. Adv Mar Biol. 2012;62:113–82.PubMed 

    Google Scholar 
    Seutin G, White BN, Boag PT. Preservation of avian blood and tissue samples for DNA analyses. Can J Zool. 1991;69:82–90.CAS 

    Google Scholar 
    Abraham AC, Gochfeld DJ, Macartney K, Mellow A, Lesser MP, Slattery M. Biochemical variability in sponges across the Caribbean basin. Invertebr Biol. 2021;140:e12341.
    Google Scholar 
    Sunagawa S, Woodley CM, Medina M. Threatened corals provide underexplored microbial habitats. PLoS One. 2010;5:e9554.PubMed 
    PubMed Central 

    Google Scholar 
    Parada AE, Needham DM, Fuhrman JA. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol. 2016;18:1403–14.CAS 
    PubMed 

    Google Scholar 
    Apprill A, McNally S, Parsons R, Weber L. Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton. Aquat Microb Ecol. 2015;75:129–37.
    Google Scholar 
    Simion P, Phillippe H, Baurain D, Jager M, Richter RJ, Di Franco A, et al. A Large and consistent phylogenomic dataset supports sponges as the sister group to all other animals. Curr Biol. 2017;27:958–67.CAS 
    PubMed 

    Google Scholar 
    Katoh K, Misawa K, Kuma KI, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002;30:3059–66.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Oksanen J, Simpson GL, Blanchet FG, Kindt R, Legendre P, Minchin PR, et al. vegan: Community Ecology Package. R package version 2.5-5. https://CRAN.R-project.org/package=vegan. Released May, 2019.Pinheiro J, Bates D, DebRoy S, Sarkar D, EISPACK Authors, Heisterkamp S, et al. nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-155. https://svn.r-project.org/R-packages/trunk/nlme/. Released Jan, 2022.Kindt R, Coe R. Tree diversity analysis. A manual and software for common statistical methods for ecological and biodiversity studies. World Agroforestry Centre, ICRAF, 2005. https://www.worldagroforestry.org/publication/tree-diversity-analysis-manual-and-software-common-statistical-methods-ecological-and.Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550.PubMed 
    PubMed Central 

    Google Scholar 
    Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Westbrook A, Ramsdell J, Schuelke T, Normington L, Bergeron RD, Thomas WK, et al. PALADIN: protein alignment for functional profiling whole metagenome shotgun data. Bioinformatics. 2017;33:1473–8.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Robinson MD, McCarthy DG, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26:139–40.CAS 
    PubMed 

    Google Scholar 
    Li D, Luo R, Liu C-M, Leung C-M, Ting H-F, Sadakane K, et al. MEGAHIT v1.0: A fast and scalable metagenome assembler driven by advanced methodologies and community practices. Methods. 2016;102:3–11.CAS 
    PubMed 

    Google Scholar 
    Li H, Durbin R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics. 2009;25:1754–60.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Blin K, Shaw S, Kautsar SA, Medema MH, Weber T. The antiSMASH database version 3: increased taxonomic coverage and new query features for modular enzymes. Nucleic Acids Res. 2009;49:D639–43.
    Google Scholar 
    Conte-Jerpe IE, Thompson PD, Wong CWM, Oliveira NL, Duprey NN, Moynihan MA, et al. Trophic strategy and bleaching resistance in reef-building corals. Sci Adv. 2020;6:eaaz5443.
    Google Scholar 
    Jackson AL, Inger R, Parnell AC, Bearhop S. Comparing isotopic niche widths among and within communities: SIBER-Stable Isotope Bayesian Ellipses. Anim Ecol. 2011;80:595–602.
    Google Scholar 
    Thomas T, Moitinho-Silva L, Lurgi M, Björk JR, Easson C, Astudillo-Garcia C, et al. Diversity, structure and convergent evolution of the global sponge microbiome. Nat Comm. 2016;7:11870.CAS 

    Google Scholar 
    Erwin PM, Coma R, López-Sendino P, Serrano E, Ribes M. Stable symbionts across the HMA-LMA dichotomy: low seasonal and inter-annual variation in sponge-associated bacteria from taxonomically diverse hosts. FEMS Microbiol Ecol. 2015;91:fiv115.PubMed 

    Google Scholar 
    Moitinho-Silva L, Steinert G, Nielsen S, Hardoim CCP, Wu Y-C, McCormack GP. Predicting the HMA-LMA status in marine sponges by machine learning. Front Microbiol. 2017;8:752.PubMed 
    PubMed Central 

    Google Scholar 
    Campana S, Demey C, Busch K, Hentschel U, Muyzer G, de Goeij J. Marine sponges maintain stable bacterial communities between reef sites with different coral to algae cover ratios. FEMS Microbiol Ecol. 2021;97:fiab115.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Freeman CJ, Thacker RW. Complex interactions between marine sponges and their symbiotic microbial communities. Limnol Oceanogr. 2011;56:1577–86.
    Google Scholar 
    Siegel A, Kamke J, Hochmuth T, Piel J, Richter M, Liang C, et al. Single-cell genomic reveals the lifestyle of Poribacteria, a candidate phylum symbiotically associated with marine sponges. ISME J. 2011;5:61–70.
    Google Scholar 
    Bayer K, Jahn MT, Slaby BM, Moitinho-Silva L, Hentschel U. Marine sponges as Chloroflexi hot spots: genomic insights and high resolution visualization of an abundant and diverse symbiotic clade. mSystems. 2018;3:e00150–18.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Fan L, Reynolds D, Liu M, Thomas T. Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts. Proc Natl Acad Sci USA. 2012;109:1878–87.
    Google Scholar 
    Ribes M, Jiménez E, Yahel G, López-Sendino P, Diez B, Massana R, et al. Functional convergence of microbes associated with temperate marine sponges. Environ Microbiol. 2012;14:1224–39.CAS 
    PubMed 

    Google Scholar 
    Thomas T, Rusch D, DeMaere MZ, Yung PY, Lewis M, Halpern A, et al. Functional genomic signatures of sponge bacteria reveal unique and shared features of symbiosis. ISME J. 2010;4:1557–67.CAS 
    PubMed 

    Google Scholar 
    Fiore CL, Labrie M, Jarett JK, Lesser MP. Transcriptional activity of the giant barrel sponge, Xestospongia muta holobiont: molecular evidence for metabolic interchange. Front Microbiol. 2015;6:364.PubMed 
    PubMed Central 

    Google Scholar 
    Engel S, Pawlik JR. Allelopathic activities of sponge extracts. Mar Ecol Prog Ser. 2000;207:273–82.
    Google Scholar 
    Gochfeld DJ, Kamel HN, Olson JB, Thacker RW. Trade-offs in defensive metabolite production but not ecological function in healthy and diseased sponges. J Chem Ecol. 2012;38:451–62.CAS 
    PubMed 

    Google Scholar 
    van Duyl FC, Mueller B, Meesters EH. Spatio-temporal variation in stable isotopic signatures (δ13C and δ15N) of sponges on the Saba Bank. PeerJ. 2018;6:e5460.PubMed 
    PubMed Central 

    Google Scholar 
    Fiore CL, Baker DM, Lesser MP. Nitrogen biogeochemistry in the Caribbean sponge, Xestospongia muta: a source or sink of dissolved inorganic nitrogen? PLoS One. 2013;8:e72961.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Hudspith M, de Goeij JM, Streekstra M, Kornder NA, Bougoure J, Guagliardo P, et al. Harnessing solar power: photoautotrophy supplements the diet of a low-light dwelling sponge. ISME J. 2022; https://doi.org/10.1038/s41396-022-01254-3.Shih JL, Selph KE, Wall CB, Wallsgrove NJ, Lesser MP, Popp BN. Trophic ecology of the tropical Pacific sponge Mycale gradis inferred from amino acid compound-specific isotopic analyses. Microb Ecol. 2020;79:495–510.CAS 
    PubMed 

    Google Scholar 
    Macartney KJ, Slattery M, Lesser MP. Trophic ecology of Caribbean sponges in the mesophotic zone. Limnol Oceanogr. 2021;66:1113–24.CAS 

    Google Scholar 
    Southwell MW, Popp BN, Martens CS. Nitrification controls on fluxes and isotopic composition of nitrate from Florida Keys sponges. Mar Chem. 2008;108:96–108.CAS 

    Google Scholar 
    Lamb K, Swart PK. The carbon and nitrogen isotopic values of particulate organic material from the Florida Keys: a temporal and spatial study. Coral Reefs. 2008;27:351–62.
    Google Scholar 
    Ferrier-Pagès C, Leal MG. Stable isotopes as tracers of trophic interactions in marine mutualistic symbioses. Ecol Evol. 2019;9:723–40.PubMed 

    Google Scholar 
    McMurray SE, Stubler AD, Erwin PM, Finelli CM, Pawlik JR. A test of the sponge-loop hypothesis for emergent Caribbean reef sponges. Mar Ecol Prog Ser. 2018;588:1–14.CAS 

    Google Scholar 
    Freeman CJ, Easson CG, Baker DM. Metabolic diversity and niche structure in sponges from the Miskito Cays, Honduras. PeerJ. 2014;2:e695.PubMed 
    PubMed Central 

    Google Scholar 
    Freeman CJ, Easson CG, Matterson KO, Thacker RW, Baker DM, Paul VJ. Microbial symbionts and ecological divergence of Caribbean sponges: a new perspective on an ancient association. ISME J. 2020;14:1571–83.PubMed 
    PubMed Central 

    Google Scholar 
    Poppell E, Weisz J, Spicer L, Massaro A, Hill A, Hill M. Sponge heterotrophic capacity and bacterial community structure in high‐and low‐microbial abundance sponges. Mar Ecol. 2014;35:414–24.
    Google Scholar 
    Morganti TM, Ribes M, Yahel G, Coma R. Size is the major determinant of pumping rates in marine sponges. Front Physiol. 2019;10:1474.PubMed 
    PubMed Central 

    Google Scholar 
    Rix L, Ribes M, Coma R, Jahn MT, de Goeij JM, van Oevelen D, et al. Heterotrophy in the earliest gut: a single-cell view of heterotrophic carbon and nitrogen assimilation in sponge-microbe symbioses. ISME J. 2020;14:2554–67.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    O’Brien PA, Tan S, Yang C, Frade PR, Andreakis N, Smith HA, et al. Diverse coral reef invertebrates exhibit patterns of phylosymbiosis. ISME J. 2020;14:2211–22.PubMed 
    PubMed Central 

    Google Scholar 
    Erwin PM, Thacker RW. Incidence and identity of photosynthetic symbionts in Caribbean coral reef sponge assemblages. J Mar Biol Assoc UK. 2007;87:1683–92.CAS 

    Google Scholar 
    Palumbi SR. Tactics of acclimation: morphological changes of sponges in an unpredictable environment. Science. 1984;225:1478–80.CAS 
    PubMed 

    Google Scholar 
    Slattery M, Gochfeld DJ, Diaz MC, Thacker RW, Lesser MP. Variability in chemical defense across a shallow to mesophotic depth gradient in the Caribbean sponge Plakortis angulospiculatus. Coral Reefs. 2016;35:11–22.
    Google Scholar 
    Morganti T, Coma R, Yahel G, Ribes M. Trophic niche separation that facilitates co‐existence of high and low microbial abundance sponges is revealed by in situ study of carbon and nitrogen fluxes. Limnol Oceanogr. 2017;62:1963–83.CAS 

    Google Scholar 
    Maldonado M. Sponge waste that fuels marine oligotrophic food webs: a re-assessment of its origin and nature. Mar Ecol. 2016;37:477–91.
    Google Scholar  More

  • in

    Acoustic and visual cetacean surveys reveal year-round spatial and temporal distributions for multiple species in northern British Columbia, Canada

    Williams, R. et al. Prioritizing global marine mammal habitats using density maps in place of range maps. Ecography 37, 212–220 (2014).
    Google Scholar 
    Tyack, P. L. & Clark, C. W. Communication and acoustic behavior of dolphins and whales in Hearing by whales and dolphins 156–224 (Springer, 2000).Davis, G. E. et al. Exploring movement patterns and changing distributions of baleen whales in the western North Atlantic using a decade of passive acoustic data. Glob. Change Biol. 26, 4812 (2020).ADS 

    Google Scholar 
    Lomac-MacNair, K. S. et al. Marine mammal visual and acoustic surveys near the Alaskan Colville River Delta. Polar Biol. 42, 441–448 (2018).
    Google Scholar 
    Keen, E., Hendricks, B., Wray, J., Alidina, H. & Picard, C. Integrating passive acoustic and visual surveys for marine mammals in coastal habitats in 176th Meeting of Acoustical Society of America. 1 edn.Gregr, E. J., Baumgartner, M. F., Laidre, K. L. & Palacios, D. M. Marine mammal habitat models come of age: The emergence of ecological and management relevance. Endang. Species Res. 22, 205–212 (2013).
    Google Scholar 
    Hastie, G. D., Wilson, B., Wilson, L., Parsons, K. M. & Thompson, P. M. Functional mechanisms underlying cetacean distribution patterns: Hotspots for bottlenose dolphins are linked to foraging. Mar. Biol. 144, 397–403 (2004).
    Google Scholar 
    Lambert, C., Mannocci, L., Lehodey, P. & Ridoux, V. Predicting cetacean habitats from their energetic needs and the distribution of their prey in two contrasted tropical regions. PLoS ONE 9, e105958 (2014).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Huot, Y. et al. Does chlorophyll a provide the best index of phytoplankton biomass for primary productivity studies?. Biogeosci. Discuss. 4, 707–745 (2007).ADS 

    Google Scholar 
    Etnoyer, P. et al. Sea-surface temperature gradients across blue whale and sea turtle foraging trajectories off the Baja California Peninsula, Mexico. Deep Sea Res. II 53, 340–358 (2006).ADS 

    Google Scholar 
    Shabangu, F. W. et al. Seasonal occurrence and diel calling behaviour of Antarctic blue whales and fin whales in relation to environmental conditions off the west coast of South Africa. J. Mar. Syst. 190, 25–39 (2019).
    Google Scholar 
    Haida Nation & Parks Canada Agency. Gwaii Haanas Gina ’Waadluxan Kilguhlga. Land-Sea-People Management Plan. 33 (© Council of the Haida Nation and Her Majesty the Queen in Right of Canada, represented by the Chief Executive Officer of Parks Canada, 2018).Ford, J. K. B. Marine Mammals of British Columbia. (Royal BC Museum, 2014).Allen, A. S., Yurk, H., Vagle, S., Pilkington, J. & Canessa, R. The underwater acoustic environment at SGaan Kinghlas-Bowie Seamount Marine Protected Area: Characterizing vessel traffic and associated noise using satellite AIS and acoustic datasets. Mar. Pollut. Bull. 128, 82–88 (2018).CAS 
    PubMed 

    Google Scholar 
    Ainslie, M. A. Principles of Sonar Performance Modeling. (Springer, 2010).Collins, M. D. A split-step Padé solution for the parabolic equation method. J. Acoust. Soc. Am. 93, 1736–1742 (1993).ADS 

    Google Scholar 
    Porter, M. B. & Bucker, H. P. Gaussian beam tracing for computing ocean acoustic fields. J. Acoust. Soc. Am. 82, 1349–1359 (1987).ADS 

    Google Scholar 
    Mouy, X., MacGillivray, A. O., Vallarta, J. H., Martin, B. & Delarue, J. J.-Y. Ambient Noise and Killer Whale Monitoring near Port Metro Vancouver’s Proposed Terminal 2 Expansion Site: July–September 2012. (Technical report by JASCO Applied Sciences for Hemmera, 2012).Ford, J. et al. Distribution and relative abundance of cetaceans in western Canadian waters from ship surveys, 2002–2008. Can. Tech. Rep. Fish. Aquat. Sci. 2913, 51 (2010).
    Google Scholar 
    Wright, B. M., Nichol, L. M. & Doniol-Valcroze, T. Spatial density models of cetaceans in the Canadian Pacific estimated from 2018 ship-based surveys. DFO Can. Sci. Advis. Sec. Res. Doc. 2021, 49 (2021).
    Google Scholar 
    Devred, E., Hardy, M. & Hannah, C. Satellite observations of the Northeast Pacific Ocean. Can. Tech. Rep. Hydrogr. Ocean Sci. 335, 46 (2021).
    Google Scholar 
    Saha, K. et al. NOAA National centers for environmental information. Dataset https://doi.org/10.7289/v52j68xx (2018).Article 

    Google Scholar 
    NASA Goddard Space Flight Center, Ocean Ecology Laboratory & Ocean Biology Processing Group. (NASA OB.DAAC, Greenbelt, MD, USA. https://doi.org/10.5067/AQUA/MODIS/L3B/CHL/2018. Accessed 3 Feb 2021.Wood, S. N. Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. J. R. Stat. Soc. B Stat. Methodol. 73, 3–36 (2011).MathSciNet 
    MATH 

    Google Scholar 
    R Core Team. R: A language and environment for statistical computing. R foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ (2021).Ogle, D. H., Wheeler, P. & Dinno, A. FSA: Fisheries Stock Analysis. R package version 0.8.32. https://github.com/droglenc/FSA (2021).Payne, R. S. & McVay, S. Songs of humpback whales. Science 173, 585–597 (1971).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Rekdahl, M. L. et al. Non-song social call bouts of migrating humpback whales. J. Acoust. Soc. Am. 137, 3042–3053 (2015).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Oswald, J. N., Rankin, S. & Barlow, J. To whistle or not to whistle? Geographic variation in the whistling behavior of small odontocetes. Aquat. Mamm. 34, 288–302 (2008).
    Google Scholar 
    Rankin, S., Oswald, J., Barlow, J. P. & Lammers, M. Patterned burst-pulse vocalizations of the northern right whale dolphin, Lissodelphis borealis. J. Acoust. Soc. Am. 121, 1213–1218. https://doi.org/10.1121/1.2404919 (2007).Article 
    ADS 
    PubMed 

    Google Scholar 
    Arranz, P. et al. Discrimination of fast click-series produced by tagged Risso’s dolphins (Grampus griseus) for echolocation or communication. J. Exp. Biol. 219, 2898–2907. https://doi.org/10.1242/jeb.144295 (2016).Article 
    CAS 
    PubMed 

    Google Scholar 
    Halpin, L. R., Towers, J. R. & Ford, J. K. First record of common bottlenose dolphin (Tursiops truncatus) in Canadian Pacific waters. Mar. Biodivers. Rec. 11, 1–5 (2018).
    Google Scholar 
    Nikolich, K. & Towers, J. R. Vocalizations of common minke whales (Balaenoptera acutorostrata) in an eastern North Pacific feeding ground. Bioacoustics 29, 97–108 (2020).
    Google Scholar 
    Money, J. H. & Trites, A. W. A preliminary assessment of the status of marine mammal populations and associated research needs for the west coast of Canada. Report No. Final Report, 80 (Fisheries and Oceans Canada, 1998).Gregr, E. J. & Trites, A. W. Predictions of critical habitat for five whale species in the waters of coastal British Columbia. Can. J. Fish. Aquat. Sci. 58, 1265–1285 (2001).
    Google Scholar 
    Ou, H., Au, W. W. L., Van Parijs, S., Oleson, E. M. & Rankin, S. Discrimination of frequency-modulated Baleen whale downsweep calls with overlapping frequencies. J. Acoust. Soc. Am. 137, 3024–3032. https://doi.org/10.1121/1.4919304 (2015).Article 
    ADS 
    PubMed 

    Google Scholar 
    Mellinger, D. K., Stafford, K. M., Moore, S. E., Dziak, R. P. & Matsumoto, H. An overview of fixed passive acoustic observation methods for cetaceans. Oceanography 20, 36–45 (2007).
    Google Scholar 
    Stafford, K. M., Citta, J. J., Moore, S. E., Daher, M. A. & George, J. E. Environmental correlates of blue and fin whale call detections in the North Pacific Ocean from 1997 to 2002. Mar. Ecol. Prog. Ser. 395, 37–53 (2009).ADS 

    Google Scholar 
    Burnham, R., Duffus, D. & Mouy, X. The presence of large whale species in Clayoquot Sound and its offshore waters. Cont. Shelf Res. 177, 15–23 (2019).ADS 

    Google Scholar 
    Burtenshaw, J. C. et al. Acoustic and satellite remote sensing of blue whale seasonality and habitat in the Northeast Pacific. Deep Sea Res. II 51, 967–986 (2004).ADS 

    Google Scholar 
    Calambokidis, J., Barlow, J., Ford, J. K. B., Chandler, T. E. & Douglas, A. B. Insights into the population structure of blue whales in the Eastern North Pacific from recent sightings and photographic identification. Mar. Mamm. Sci. 25, 816–832 (2009).
    Google Scholar 
    Jackson, J. M., Thomson, R. E., Brown, L. N., Willis, P. G. & Borstad, G. A. Satellite chlorophyll off the British Columbia Coast, 1997–2010. J. Geophys. Res. Oceans 120, 4709–4728 (2015).ADS 

    Google Scholar 
    Evans, R., English, P. A., Anderson, S. C., Gauthier, S. & Robinson, C. L. Factors affecting the seasonal distribution and biomass of E. pacifica and T. spinifera along the Pacific coast of Canada: A spatiotemporal modelling approach. PLoS ONE 16, e0249818 (2021).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Moore, S. E., Watkins, W. A., Daher, M. A., Davies, J. R. & Dahlheim, M. E. Blue whale habitat associations in the Northwest Pacific: Analysis of remotely-sensed data using a Geographic Information System. Oceanography 15, 1–10 (2002).
    Google Scholar 
    Lockyer, C. Review of Baleen Whale (Mysticeti) reproduction and implications for management. Rep. Int. Whal. Commn Spec. Issue 6, 27–50 (1984).
    Google Scholar 
    Ohsumi, S. M. N. Growth of fin whale in the Northern Pacific Ocean. Sci. Rep. Whale Res. Inst. 13, 97–133 (1958).
    Google Scholar 
    Watkins, W. A. et al. Seasonality and distribution of whale calls in the North Pacific. Oceanography 13, 62–67 (2000).
    Google Scholar 
    Watkins, W. A., Tyack, P., Moore, K. E. & Bird, J. E. The 20-Hz signals of finback whales (Balaenoptera physalus). J. Acoust. Soc. Am. 82, 1901–1912 (1987).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Stafford, K. M., Mellinger, D. K., Moore, S. E. & Fox, C. G. Seasonal variability and detection range modeling of baleen whale calls in the Gulf of Alaska, 1999–2002. J. Acoust. Soc. Am. 122, 3378–3390 (2007).ADS 
    PubMed 

    Google Scholar 
    Koot, B. Winter Behaviour and Population Structure of Fin Whales (Balaenoptera physalus) in British Columbia inferred from passive acoustic data (University of British Columbia, 2015).
    Google Scholar 
    Pilkington, J. F., Stredulinsky, E. H., Abernethy, R. M. & Ford, J. K. B. Patterns of Fin whale (Balaenoptera physalus) Seasonality and Relative Distribution in Canadian Pacific Waters Inferred from Passive Acoustic Monitoring. DFO Can. Sci. Advis. Sec. Res. Doc. (2018).Best, B. D., Fox, C. H., Williams, R., Halpin, P. H. & Paquet, P. C. Updated Marine Mammal Distribution and Abundance Estimates in British Columbia (Springer, 2015).
    Google Scholar 
    Clarke, C. & Jamieson, G. Identification of ecologically and biologically significant areas in the Pacific North Coast integrated management area: Phase II: Final report. Can. Tech. Rep. Fish. Aquat. Sci. 2678, 59 (2006).
    Google Scholar 
    Nichol, L. M. et al. Distribution, movements and habitat fidelity patterns of Fin Whales (Balaenoptera physalus) in Canadian Pacific Waters. DFO Can. Sci. Advis. Sec. Res. Doc. (2018).Nichol, L. M. & Ford, J. K. B. Information in Support of the Identification of Habitat of Special Importance to Fin Whales (Balaenoptera physalus) in Canadian Pacific Waters. DFO Can. Sci. Advis. Sec. Res. Doc. (2018).Mizroch, S. A., Rice, D. W., Zwiefelhofer, D., Waite, J. & Perryman, W. L. Distribution and movements of fin whales in the North Pacific Ocean. Mammal Rev. 39, 193–227 (2009).
    Google Scholar 
    Širović, A., Williams, L. N., Kerosky, S. M., Wiggins, S. M. & Hildebrand, J. A. Temporal separation of two fin whale call types across the eastern North Pacific. Mar. Biol. 160, 47–57 (2013).PubMed 

    Google Scholar 
    Flinn, R. D., Trites, A. W., Gregr, E. J. & Perry, R. I. Diets of fin, sei, and sperm whales in British Columbia: an analysis of commercial whaling records, 1963–1967. Mar. Mamm. Sci. 18, 663–679 (2002).
    Google Scholar 
    Barnes, R. S. K. & Hughes, R. N. An Introduction to Marine Ecology (Wiley, 1999).
    Google Scholar 
    Romagosa, M. et al. Food talks: 40-hz fin whale calls are associated with prey biomass. Proc. R. Soc. B 288, 20211156 (2021).PubMed 
    PubMed Central 

    Google Scholar 
    Gregr, E. J., Nichol, L., Ford, J. K., Ellis, G. & Trites, A. W. Migration and population structure of northeastern Pacific whales off coastal British Columbia: An analysis of commercial whaling records from 1908–1967. Mar. Mamm. Sci. 16, 699–727 (2000).
    Google Scholar 
    Williams, R. & Thomas, L. Distribution and abundance of marine mammals in the coastal waters of British Columbia, Canada. J. Cetac. Res. Manage. 9, 15 (2007).
    Google Scholar 
    Dalla Rosa, L., Ford, J. K. & Trites, A. W. Distribution and relative abundance of humpback whales in relation to environmental variables in coastal British Columbia and adjacent waters. Contin. Shelf Res. 36, 89–104 (2012).ADS 

    Google Scholar 
    Winn, H. E. & Winn, L. K. The song of the humpback whale Megaptera novaeangliae in the West Indies. Mar. Biol. 47, 97–114. https://doi.org/10.1007/BF00395631 (1978).Article 

    Google Scholar 
    Baker, C. S. et al. Population characteristics and migration of summer and late-season humpback whales (Megaptera novaeangliae) in southeastern Alaska. Mar. Mamm. Sci. 1, 304–323 (1985).ADS 

    Google Scholar 
    McSweeney, D., Chu, K., Dolphin, W. & Guinee, L. North Pacific humpback whale songs: A comparison of southeast Alaskan feeding ground songs with Hawaiian wintering ground songs. Mar. Mamm. Sci. 5, 139–148 (1989).
    Google Scholar 
    Norris, T. F., McDonald, M. & Barlow, J. Acoustic detections of singing humpback whales (Megaptera novaeangliae) in the eastern North Pacific during their northbound migration. J. Acoust. Soc. Am. 106, 506–514 (1999).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Clark, C. W. & Clapham, P. J. Acoustic monitoring on a humpback whale (Megaptera novaeangliae) feeding ground shows continual singing into late spring. Proc. R. Soc. Lond. B 271, 1051–1057 (2004).
    Google Scholar 
    Stimpert, A. K., Peavey, L. E., Friedlaender, A. S. & Nowacek, D. P. Humpback whale song and foraging behavior on an Antarctic feeding ground. PLoS ONE 7, e51214 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kowarski, K., Evers, C., Moors-Murphy, H., Martin, B. & Denes, S. L. Singing through winter nights: Seasonal and diel occurrence of humpback whale (Megaptera novaeangliae) calls in and around the Gully MPA, offshore eastern Canada. Mar. Mamm. Sci. 34, 169–189 (2018).
    Google Scholar 
    Nichol, L. M., Abernethy, R., Flostrand, L., Lee, T. S. & Ford, J. K. B. Information relevant for the identification of critical habitats of north pacific humpback whales (Megaptera novaeangliae) in British Columbia. DFO Can. Sci. Advis. Sec. Res. Doc. (2010).Williams, R., Erbe, C., Ashe, E. & Clark, C. W. Quiet (er) marine protected areas. Mar. Pollut. Bull. 100, 154–161 (2015).CAS 
    PubMed 

    Google Scholar 
    Gaston, A. J., Pilgrim, N. G. & Pattison, V. Humpback Whale (Megaptera novaeangliae) observations in Laskeek Bay, western Hecate Strait, in spring and early summer, 1990–2018. Can. Field Nat. 133, 263–269 (2019).
    Google Scholar 
    Robinson, C. L., Gower, J. F. & Borstad, G. Twenty years of satellite observations describing phytoplankton blooms in seas adjacent to Gwaii Haanas National Park Reserve, Canada. Can. J. Remote Sens. 30, 36–43 (2004).ADS 

    Google Scholar 
    Swartz, S. L., Taylor, B. L. & Rugh, D. J. Gray whale Eschrichtius robustus population and stock identity. Mamm. Rev. 36, 66–84 (2006).
    Google Scholar 
    Gaston, A. J. & Heise, K. Results of cetacean observations in Laskeek Bay, 1990–2003. Laskeek Bay Res. 55, 1–10 (2004).
    Google Scholar 
    Ford, J. K. et al. New insights into the northward migration route of gray whales between Vancouver Island, British Columbia, and southeastern Alaska. Mar. Mamm. Sci. 29, 325–337 (2013).
    Google Scholar 
    Burnham, R. E. & Duffus, D. A. The use of passive acoustic monitoring as a census tool of gray whale (Eschrichtius robustus) migration. Ocean Coast. Manag. 188, 105070 (2020).
    Google Scholar 
    Best, P. B. Social organization in sperm whales. In Physeter macrocephalus in Behavior of Marine Animals (eds Winn, H. E. & Olla, B. L.) 227–289 (Springer, 1979).
    Google Scholar 
    Jaquet, N. & Gendron, D. Distribution and relative abundance of sperm whales in relation to key environmental features, squid landings and the distribution of other cetacean species in the Gulf of California, Mexico. Mar. Biol. 141, 591–601 (2002).
    Google Scholar 
    Rice, D. W. Sperm whale Physeter macrocephalus Linnaeus, 1758. Handb. Mar. Mamm. 4, 177–233 (1989).
    Google Scholar 
    Whitehead, H. & Arnbom, T. Social organization of sperm whales off the Galapagos Islands, February–April 1985. Can. J. Zool. 65, 913–919 (1987).
    Google Scholar 
    Whitehead, H. Sperm whale: Physeter macrocephalus. In Encyclopedia of Marine Mammals 3rd edn (eds Würsig, B. et al.) 919–925 (Academic Press, 2018).
    Google Scholar 
    Mizroch, S. A. & Rice, D. W. Ocean nomads: Distribution and movements of sperm whales in the North Pacific shown by whaling data and Discovery marks. Mar. Mamm. Sci. 29, E136–E165 (2013).
    Google Scholar 
    Diogou, N. et al. Sperm whale (Physeter macrocephalus) acoustic ecology at Ocean Station PAPA in the Gulf of Alaska-Part 2: Oceanographic drivers of interannual variability. Deep Sea Res. I 150, 103044 (2019).
    Google Scholar 
    Ford, J. K. & Ellis, G. M. You are what you eat: Foraging specializations and their influence on the social organization and behavior of killer whales. in Primates and Cetaceans 75–98 (Springer, 2014).Ford, J. K. B. et al. Habitats of special importance to resident killer whales (Orcinus orca) off the West Coast of Canada. DFO Can. Sci. Advis. Sec. Res. Doc. (2017).Ford, J. K. B., Stredulinsky, E. H., Ellis, G. M., Durban, J. W. & Pilkington, J. F. Offshore Killer whales in Canadian pacific waters: Distribution, seasonality, foraging ecology, population status and potential for recovery. DFO Can. Sci. Advis. Sec. Res. Doc. (2014).Nichol, L. M. & Shackleton, D. M. Seasonal movements and foraging behaviour of northern resident killer whales (Orcinus orca) in relation to the inshore distribution of salmon (Oncorhynchus spp.) in British Columbia. Can. J. Zool. 74, 983–991 (1996).
    Google Scholar 
    Olesiuk, P. F., Ellis, G. M. & Ford, J. K. Life History and Population Dynamics of Northern Resident Killer Whales (Orcinus orca) in British Columbia (Canadian Science Advisory Secretariat Ottawa, 2005).
    Google Scholar 
    Newman, K. & Springer, A. Nocturnal activity by mammal-eating killer whales at a predation hot spot in the Bering Sea. Mar. Mamm. Sci. 24, 990 (2008).
    Google Scholar 
    Ford, J. K. B. et al. Dietary specialization in two sympatric populations of killer whales (Orcinus orca) in coastal British Columbia and adjacent waters. Can. J. Zool. 76, 1456–1471 (1998).
    Google Scholar 
    Barrett-Lennard, L. G., Ford, J. K. B. & Heise, K. A. The mixed blessing of echolocation: Differences in sonar use by fish-eating and mammal-eating killer whales. Anim. Behav. 51, 553–565 (1996).
    Google Scholar 
    Deecke, V. B., Ford, J. K. B. & Slater, P. J. B. The vocal behaviour of mammal-eating killer whales: Communicating with costly calls. Anim. Behav. 69, 395–405 (2005).
    Google Scholar 
    Ford, J. K. B. Call traditions and vocal dialects of killer whales (Orcinus orca) in British Columbia Ph.D. thesis, University of British Columbia (1984).Baird, R. W. Status of killer whales, Orcinus orca, Canada. Can. Field. Nat. 115, 676–701 (2001).
    Google Scholar 
    Ford, J. K. B., Stredulinsky, E. H., Towers, J. R. & Ellis, G. M. Information in Support of the Identification of Critical Habitat for Transient Killer Whales (Orcinus orca) off the West Coast of Canada. DFO Can. Sci. Advis. Sec. Res. Doc. (2013).Tyack, P. L., Johnson, M., Soto, N. A., Sturlese, A. & Madsen, P. T. Extreme diving of beaked whales. J. Exp. Biol. 209, 4238–4253 (2006).PubMed 

    Google Scholar 
    Baumann-Pickering, S. et al. Species-specific beaked whale echolocation signals. J. Acoust. Soc. Am. 134, 2293–2301 (2013).ADS 
    PubMed 

    Google Scholar 
    Pike, G. C. Two records of Berardius bairdi from the coast of British Columbia. J. Mammal. 34, 98–104 (1953).
    Google Scholar 
    Pike, G. C. & MacAskie, I. Marine mammals of British Columbia. Fish. Res. Board Can. Bull. 171, 1–10 (1969).
    Google Scholar 
    Willis, P. M. & Baird, R. W. Sightings and strandings of beaked whales on the west coast of. Aquat. Mamm. 24, 21–25 (1998).
    Google Scholar 
    Jefferson, T. A. Phocoenoides dalli. Mamm. Spec. https://doi.org/10.2307/3504170 (1988).Article 

    Google Scholar 
    Boyd, C. et al. Estimation of population size and trends for highly mobile species with dynamic spatial distributions. Divers. Distrib. 24, 1–12 (2018).
    Google Scholar 
    Carretta, J. V., Taylor, B. L. & Chivers, S. J. Abundance and depth distribution of harbor porpoise (Phocoena phocoena) in northern California determined from a 1995 ship survey. Fish. Bull. 99, 29–29 (2001).
    Google Scholar 
    Willis, P. M. & Baird, R. W. Status of the dwarf sperm whale, Kogia simus, with special reference to Canada. Can. Field Nat. 112, 114–125 (1998).
    Google Scholar 
    Kyhn, L. A. et al. Clicking in a killer whale habitat: Narrow-band, high-frequency biosonar cliks of harbour porpoise (Phocoena phocoena) and Dall’s porpoise (Phocoenoides dalli). PLoS ONE 8, e63763 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Madsen, P., Carder, D., Bedholm, K. & Ridgway, S. Porpoise clicks from a sperm whale nose—Convergent evolution of 130 kHz pulses in toothed whale sonars?. Bioacoustics 15, 195–206 (2005).
    Google Scholar 
    Merkens, K. et al. Clicks of dwarf sperm whales (Kogia sima). Mar. Mamm. Sci. 34, 963–978 (2018).
    Google Scholar 
    Griffiths, E. T. et al. Detection and classification of narrow-band high frequency echolocation clicks from drifting recorders. J. Acoust. Soc. Am. 147, 3511–3522 (2020).ADS 
    PubMed 

    Google Scholar 
    Baird, R. W. & Stacey, P. J. Status of Risso’s Dolphin, Grampus griseus, in Canada. Naturalist 5, 233142 (1991).
    Google Scholar 
    Benoit-Bird, K. J. & Au, W. W. Prey dynamics affect foraging by a pelagic predator (Stenella longirostris) over a range of spatial and temporal scales. Behav. Ecol. Sociobiol. 53, 364–373 (2003).
    Google Scholar 
    Benoit-Bird, K. J., Würsig, B. & Mfadden, C. J. Dusky dolphin (Lagenorhynchus obscurus) foraging in two different habitats: active acoustic detection of dolphins and their prey. Mar. Mamm. Sci. 20, 215–231 (2004).
    Google Scholar 
    Soldevilla, M. S., Wiggins, S. M. & Hildebrand, J. A. Spatial and temporal patterns of Risso’s dolphin echolocation in the Southern California Bight. J. Acoust. Soc. Am. 127, 124–132 (2010).ADS 
    PubMed 

    Google Scholar 
    Soldevilla, M. S., Wiggins, S. M. & Hildebrand, J. A. Spatio-temporal comparison of Pacific white-sided dolphin echolocation click types. Aquat. Biol. 9, 49–62 (2010).
    Google Scholar 
    Taylor, F. The relationship of midwater trawl catches to sound scattering layers off the coast of northern British Columbia. J. Fish. Board Can. 25, 457–472 (1968).
    Google Scholar 
    Curtis, K. R., Howe, B. M. & Mercer, J. A. Low-frequency ambient sound in the North Pacific: Long time series observations. J. Acoust. Soc. Am. 106, 3189–3200 (1999).ADS 

    Google Scholar 
    Aroyan, J. L. et al. Acoustic models of sound production and propagation in Hearing by whales and dolphins 409–469 (Springer, 2000).
    Google Scholar 
    Cummings, W. C. & Thompson, P. O. Underwater sounds from the blue whale, Balaenoptera musculus. J. Acoust. Soc. Am. 50, 1193–1198 (1971).ADS 

    Google Scholar 
    McDonald, M. A., Calambokidis, J., Teranishi, A. M. & Hildebrand, J. A. The acoustic calls of blue whales off California with gender data. J. Acoust. Soc. Am. 109, 1728–1735 (2001).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Weirathmueller, M. J., Wilcock, W. S. D. & Soule, D. C. Source levels of fin whale 20 Hz pulses measured in the Northeast Pacific Ocean. J. Acoust. Soc. Am. 133, 741–749 (2013).ADS 
    PubMed 

    Google Scholar 
    Vihtakari, M. ggOceanMaps: Plot Data on Oceanographic Maps using ‘ggplot2’. R package version 1.2.14. https://mikkovihtakari.github.io/ggOceanMaps/ (2022). More

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    Living on the sea-coast: ranging and habitat distribution of Asiatic lions

    Study areaSituated in western India’s southwestern part of the Gujarat state, the Saurashtra region typically represents the semi-arid Gujarat-Rajputana province 4B23, which covers 11 out of 33 districts of the state. The region forms a rocky tableland (altitude 300–600 m) fringed by coastal plains with an undulating central plain broken by hills and dissected by various rivers that flow in all directions24. With the longest coastline (~ 1600 km) in India, Gujarat is endowed with rich coastal biodiversity25,26. The Saurashtra coast in Gujarat is encircled by the open sea between two Gulfs (68° 58′–71° 30′ N and 22° 15′–20° 50′ E) and divided into two segments, viz. the southwestern coast from Dwarka to Diu (~ 300 km stretch) and south-eastern coast from Diu to Bhavnagar (~ 250 km stretch)26.The Asiatic Lion Landscape covers an area of ~ 30,000 km2 (permanent lion distribution range: ~ 16,000 km2; visitation record range: ~ 14,000 km2) of varied habitat types within Saurashtra. The landscape includes five protected areas (Gir National Park, Gir Wildlife Sanctuary, Paniya Wildlife Sanctuary, Mitiyala Wildlife Sanctuary, and Girnar Wildlife Sanctuary) and other forest classes (reserved forests, protected forests, and unclassed forests).The coastal habitats extend across the districts of Bhavnagar, Amreli, Gir-Somnath, and Junagadh (Fig. 1). Within these districts (Fig. 1), the tehsils (sub-divisions/taluka) of Mangrol, Malia, Patan-Veraval, Sutrapada, Kodinar and Una are categorized under the southwestern coast (hereafter western coastal habitat), Jafrabad, Rajula, form the south-eastern coast and Mahuva and Talaja constitute the Bhavnagar coast and represent distinct lion range units (Fig. 1). The total area covered in the study is 2843 km2 on the eastern coast and 1413 km2 on the western coast (Fig. 1).The Saurashtra region is bestowed with three distinct seasons, viz. dry and hot summer (March–June), monsoon (July–October), and primarily dry winter (November–February). It receives a mean annual rainfall of ~ 600 mm, with most rainfall during the southwest monsoon27. The mean maximum and minimum temperatures are 34 °C and 19 °C, respectively28. There is a 110 km2 stretch of forests along the coast. The rest of the areas are multi-use consisting of private, industrial, pastoral and wastelands of varied ownerships. The natural vegetation primarily consists of Prosopis juliflora and Casuarina equistsetifolia. On the beach and dune areas, vegetation such as Ipomea pescaprae, Sporobolus trinules, Fimrystylis sp., Crotalaria sp., and Euphorbia nivuleria29. The mudflats along the coast are restricted to Talaja, Mahuva, Pipavav Port, Jafrabad creek, and Porbandar, sparsely covered by the Avicennia marina29. Fisheries, agriculture, horticulture, livestock rearing, and some large- and small-scale industries are the leading economies in the coastal belt.Coastal segments are characterized by the variety of vegetation, sandy beaches, small cliffs, wave-cut platforms, open and submerged dunes, minor estuaries, embankments, and transition from the open sea to gulf environment with tidal mud26,29 and also support a diverse assemblage of biodiversity25. This biodiversity is further enriched by several perennial/ephemeral rivers originating from the Gir PA (Shetrunji, Machundari, Raval, Ardak, Bhuvatirth, Shinghoda, Hiran, Saraswati, etc.)12. These rivers meet the sea at different sections of the coast, forming prominent coastal ecosystems25. The riverine tracts act as important corridors for wildlife movement9,12,30. Dispersing through these corridors, lions have started inhabiting these coastal habitats30,31.MethodsAll the research activities involved in this study on Asiatic lions were carried out after taking due permission from the Ministry of Environment, Forests & Climate Change (MoEF&CC), Government of India (Letter No.: F. No. 1-50/2018 WL) and Principal Chief Conservator of Forests (Wildlife) & Chief Wildlife Warden, Gujarat State, Gandhinagar (Letter No.: WLP 26B 781-83/2019-20). Procedures and protocols were followed as per the Standard Operating Procedures of the Gujarat Forest Department, Government of Gujarat, concerning the handling of wild animals. Qualified and experienced veterinarians and their team carried out all procedures related to radio-collaring. Moreover, the study is reported in accordance with ‘Animal Research: Reporting of In Vivo Experiments’ (ARRIVE) guidelines as applicable.A long-term lion monitoring project was initiated in 2019 by the Gujarat Forest Department to understand the movement patterns and ecology of lions in the Asiatic Lion Landscape. Looking at the heterogeneity and vastness of the coastal areas, ten individuals were carefully selected for satellite radio-collaring based on their frequent movement in different coastal habitats and monitored from 2019 to 2021.The lions were deployed with Vertex Plus GPS Collars (Vectronics Aerospace GmbH, Berlin, Germany) that weighed less than three per cent of the individual’s body weight, irrespective of age and sex. The lions were immobilized using a combination of Ketamine hydrochloride (2.2 mg per kg body weight; Ketamine, Biowet, Pulawy) and Xylazine hydrochloride (1.1 mg per kg body weight; Xylaxil, Brilliant Bio Pharma Pvt. Ltd., Telangana)32 administered intramuscularly using a gas-powered Telinject™ G.U.T 50 (Telinject Inc., Dudenhofen, Germany) dart delivery system. A blindfold was placed to protect the eyes and decrease visual stimuli33,34. Each sedated individual was sexed, aged, and measured as per the standard operating procedure (SOP) of the Gujarat Forest Department, Government of Gujarat, and recorded the data in the trapping datasheet. The radio-collars were deployed considering the neck girth of the individual, ensuring free movement of it so as not to hamper the individual’s routine activities. After deploying the radio-collar, we used the specific antidote for Xylazine, i.e., Yohimbine hydrochloride (0.1–0.15 mg per kg body weight; Yohimbe, Equimed, USA) intravenously, resulting in the total recovery of immobilized individuals32 within 5–10 min. The individuals were intensively monitored for 72 h and, after that, regularly monitored throughout the functional period of the radio-collars. The entire radio-collaring exercise was carried out by trained and experienced veterinary officers and their teams that constituted wildlife health care personnel and field staff.Each collar had a unique VHF and UHF frequency. The radio-collars were equipped with a programmable GPS schedule and configured to record the location fixes at every hour and provided the data through the constellation of low-earth-orbit Iridium satellite data service (Iridium Communications Inc., Virginia, USA) at four-hour intervals after getting activated. The data logs included location fixes in degree decimal format (latitude/longitude), speed (km/hour), altitude (meters above mean sea level), UTC timestamp (dd-mm-yyyy h:m:s), direction (degrees), and temperature (Celsius). Radio-collars were equipped with mortality sensors and a programmable drop-off activation system. Gir Hi-Tech Monitoring Unit, Sasan-Gir, Gujarat, monitored and coordinated these activities. The location data from each radio-collar was downloaded using the GPS Plus X software (Vectronics Aerospace GmbH, Berlin, Germany) in the Gir Hi-Tech Monitoring Unit (a technology-driven scientific monitoring initiative in the landscape established in 2019 at Sasan-Gir, Gujarat).Data analysisIn this study, we calculated the home range of lions resident in the coastal region using the Fixed Kernel method. We expressed them as 90% and 50% Fixed Kernel (FK) to summarize the overall home range and core area, respectively35,36,37. Additionally, the home range of lions categorized as “link lions” and lions of the protected area was summarized for comparison (Table 1).MaxEnt (version 3.4.1) stand-alone software38 was applied for fine-scaled lion distribution modelling39,40. The logistic output format was set for the MaxEnt output. 30% random lion occurrence points were used as test data to evaluate model performance. The area under the receiver operating characteristic curve (AUC) was used to evaluate the discriminative ability of the model based on the values of sensitivity (correct discrimination of true positive location points) and specificity (correct discrimination of true negative absence points)41. The Jackknife regularised training gain for the species was used to understand the effect of each variable in model building. The logical output by the MaxEnt was presented in a table format as “percent contribution” and “permutation importance” values (from 0 to 100%). Spatial inputs were prepared on the GIS platform using ArcMap (version 10.8.1, ESRI, Redlands, USA)42. Input data for MaxEnt were categorized as (i) lion occurrence data, (ii) model variables were prepared as described below:

    i.

    Occurrence data
    At the first level, inconsistent location fixes (records with missing coordinates, time stamps, and elevation) and outliers were filtered out. Next, each lion’s hourly GPS location fixes obtained from remotely monitored radio-telemetry data were randomized to overcome spatial and temporal biases. The data was reduced by taking every three-hour location fix43,44. The data was further categorized season-wise, viz. summer, monsoon and winter. This consolidated data was then subject to spatial thinning of one kilometre using SDMtoolbox (version 2.0)45,46.

    ii.

    Model variables

    The variables used for distribution modelling broadly included different categories of land use, including both natural habitats and anthropogenic factors, namely, roads and human settlement areas. All variables were rasterized at 10 m spatial resolution.Land Use Land Cover (LULC) data of Saurashtra was obtained from Bhaskaracharya National Institute for Space Applications and Geo-informatics (BISAG-N), Gandhinagar, Gujarat. The data was then further classified into 18 sub-classes—Forest, Sandy areas, Salt-affected, Saltpan, open scrub, dense scrub (Wastelands), Waterlogged, River/Stream/Drain, Lakes and Ponds, Mining/Industrial areas, Reservoir/Tanks, Mangrove/Swamp Area, Crop Land, Agriculture Plantation (horticulture and agro-forestry), Core urban, Mixed settlement, Peri-urban, Village (Fig. 2).Roads and highways were also analyzed as separate variables in the model. Roads were classified as village roads, major district roads, and state and national highways and digitized individually to estimate Euclidean distance further (Table 2). Euclidean distance from the human settlement (Core-urban, Peri-urban, villages and mixed settlement) was analyzed and taken as a separate input variable for the model. More

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    Stacked distribution models predict climate-driven loss of variation in leaf phenology at continental scales

    Wright, S. Evolution in Mendelian Populations. Genetics 16, 97–159 (1931).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    DiBattista, J. D. Patterns of genetic variation in anthropogenically impacted populations. Conserv. Genet. 9, 141–156 (2008).
    Google Scholar 
    Ellegren, H. & Galtier, N. Determinants of genetic diversity. Nat. Rev. Genet. 17, 422–433 (2016).CAS 
    PubMed 

    Google Scholar 
    Nei, M., Maruyama, T. & Chakraborty, R. The Bottleneck Effect and Genetic Variability in Populations. Evolution 29, 1–10 (1975).PubMed 

    Google Scholar 
    Frankham, R. Stress and adaptation in conservation genetics. J. Evol. Biol. 18, 750–755 (2005).CAS 
    PubMed 

    Google Scholar 
    Mimura, M. et al. Understanding and monitoring the consequences of human impacts on intraspecific variation. Evol. Appl. 10, 121–139 (2017).PubMed 

    Google Scholar 
    Whitham, T. G. et al. A framework for community and ecosystem genetics: from genes to ecosystems. Nat. Rev. Genet. 7, 510–523 (2006).CAS 
    PubMed 

    Google Scholar 
    Hughes, A., Inouye, B., Johnson, M., Underwood, N. & Vellend, M. Ecological consequences of genetic diversity. Ecol. Lett. 11, 609–623 (2008).PubMed 

    Google Scholar 
    Hughes, A. R., Stachowicz, J. J. & Williams, S. L. Morphological and physiological variation among seagrass (Zostera marina) genotypes. Oecologia 159, 725–733 (2009).PubMed 

    Google Scholar 
    Schweitzer, J. A. et al. Genetically based trait in a dominant tree affects ecosystem processes: Plant genetics impact ecosystems. Ecol. Lett. 7, 127–134 (2004).
    Google Scholar 
    Hughes, A. R. & Stachowicz, J. J. Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance. Proc. Natl Acad. Sci. USA 101, 8998–9002 (2004).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Wimp, G. M. et al. Conserving plant genetic diversity for dependent animal communities. Ecol. Lett. 7, 776–780 (2004).
    Google Scholar 
    Reusch, T. B. H., Ehlers, A., Hämmerli, A. & Worm, B. Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proc. Natl Acad. Sci. 102, 2826–2831 (2005).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Cardinale, B. J. et al. Biodiversity loss and its impact on humanity. Nature 486, 59–67 (2012).CAS 
    PubMed 

    Google Scholar 
    Salo, T. & Gustafsson, C. The Effect of Genetic Diversity on Ecosystem Functioning in Vegetated Coastal Ecosystems. Ecosystems 19, 1429–1444 (2016).
    Google Scholar 
    Zettlemoyer, M. A. & Peterson, M. L. Does Phenological Plasticity Help or Hinder Range Shifts Under Climate Change? Front. Ecol. Evol. 9, 392 (2021).
    Google Scholar 
    Fei, S. et al. Divergence of species responses to climate change. Sci. Adv. 3, e1603055 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    Yiming, L. et al. Latitudinal gradients in genetic diversity and natural selection at a highly adaptive gene in terrestrial mammals. Ecography 44, 206–218 (2021).
    Google Scholar 
    Excoffier, L., Foll, M. & Petit, R. J. Genetic Consequences of Range Expansions. Annu. Rev. Ecol. Evol. Syst. 40, 481–501 (2009).
    Google Scholar 
    Alsos, I. G. et al. Genetic consequences of climate change for northern plants. Proc. R. Soc. B Biol. Sci. 279, 2042–2051 (2012).
    Google Scholar 
    Stahl, U., Reu, B. & Wirth, C. Predicting species’ range limits from functional traits for the tree flora of North America. Proc. Natl Acad. Sci. 111, 13739–13744 (2014).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Van Nuland, M. E. et al. Intraspecific trait variation across elevation predicts a widespread tree species’ climate niche and range limits. Ecol. Evol. 10, 3856–3867 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    Peterson, M. L., Angert, A. L. & Kay, K. M. Experimental migration upward in elevation is associated with strong selection on life history traits. Ecol. Evol. 10, 612–625 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    Vitasse, Y., Signarbieux, C. & Fu, Y. H. Global warming leads to more uniform spring phenology across elevations. Proc. Natl Acad. Sci. 115, 1004–1008 (2018).CAS 
    PubMed 

    Google Scholar 
    Piao, S. et al. Plant phenology and global climate change: Current progresses and challenges. Glob. Change Biol. 25, 1922–1940 (2019).
    Google Scholar 
    Chen, I.-C., Hill, J., Ohlemüller, R., Roy, D. B. & Thomas, C. Rapid Range Shifts of Species Associated with High Levels of Climate Warming. Science 333, 1024–6 (2011).CAS 
    PubMed 

    Google Scholar 
    Pauls, S. U., Nowak, C., Bálint, M. & Pfenninger, M. The impact of global climate change on genetic diversity within populations and species. Mol. Ecol. 22, 925–946 (2013).PubMed 

    Google Scholar 
    De Kort, H. et al. Life history, climate and biogeography interactively affect worldwide genetic diversity of plant and animal populations. Nat. Commun. 12, 516 (2021).PubMed 
    PubMed Central 

    Google Scholar 
    Hampe, A. & Petit, R. J. Conserving biodiversity under climate change: the rear edge matters. Ecol. Lett. 8, 461–467 (2005).PubMed 

    Google Scholar 
    DeMarche, M. L., Doak, D. F. & Morris, W. F. Incorporating local adaptation into forecasts of species’ distribution and abundance under climate change. Glob. Change Biol. 25, 775–793 (2019).
    Google Scholar 
    Bothwell, H. M. et al. Genetic data improves niche model discrimination and alters the direction and magnitude of climate change forecasts. Ecol. Appl. 31, e02254 (2021).Syfert, M. M., Brummitt, N. A., Coomes, D. A., Bystriakova, N. & Smith, M. J. Inferring diversity patterns along an elevation gradient from stacked SDMs: A case study on Mesoamerican ferns. Glob. Ecol. Conserv. 16, e00433 (2018).
    Google Scholar 
    Mateo, R. G., Felicísimo, Á. M., Pottier, J., Guisan, A. & Muñoz, J. Do Stacked Species Distribution Models Reflect Altitudinal Diversity Patterns? PLOS ONE 7, e32586 (2012).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ferrier, S. & Guisan, A. Spatial modelling of biodiversity at the community level. J. Appl. Ecol. 43, 393–404 (2006).
    Google Scholar 
    Ware, I. M. et al. Climate-driven reduction of genetic variation in plant phenology alters soil communities and nutrient pools. Glob. Change Biol. 25, 1514–1528 (2019).
    Google Scholar 
    Endler, J. A. Geographic variation, speciation, and clines (Princeton University Press, 1977).May, R. M. & Godfrey, J. Biological Diversity: Differences between Land and Sea [and Discussion]. Philos. Trans. Biol. Sci. 343, 105–111 (1994).
    Google Scholar 
    Des Roches, S. et al. The ecological importance of intraspecific variation. Nat. Ecol. Evol. 2, 57–64 (2018).PubMed 

    Google Scholar 
    Van Nuland, M. E., Bailey, J. K. & Schweitzer, J. A. Divergent plant–soil feedbacks could alter future elevation ranges and ecosystem dynamics. Nat. Ecol. Evol. 1, 0150 (2017).
    Google Scholar 
    Richardson, A. D. et al. Influence of spring and autumn phenological transitions on forest ecosystem productivity. Philos. Trans. R. Soc. B Biol. Sci. 365, 3227–3246 (2010).
    Google Scholar 
    Richardson, A. D. et al. Influence of spring phenology on seasonal and annual carbon balance in two contrasting New England forests. Tree Physiol. 29, 321–321 (2009).CAS 
    PubMed 

    Google Scholar 
    Huntington, T. G. CO2-induced suppression of transpiration cannot explain increasing runoff. Hydrol. Process. 22, 311–314 (2008).
    Google Scholar 
    Kim, J. H. et al. Warming-Induced Earlier Greenup Leads to Reduced Stream Discharge in a Temperate Mixed Forest Catchment. J. Geophys. Res. Biogeosciences 123, 1960–1975 (2018).
    Google Scholar 
    Ware, I. M. et al. Climate-driven divergence in plant-microbiome interactions generates range-wide variation in bud break phenology. Commun. Biol. 4, 748 (2021).PubMed 
    PubMed Central 

    Google Scholar 
    Mori, A. S. et al. Biodiversity–productivity relationships are key to nature-based climate solutions. Nat. Clim. Change 11, 543–550 (2021).
    Google Scholar 
    Woolbright, S. A., Whitham, T. G., Gehring, C. A., Allan, G. J. & Bailey, J. K. Climate relicts and their associated communities as natural ecology and evolution laboratories. Trends Ecol. Evol. 29, 406–416 (2014).PubMed 

    Google Scholar 
    Naiman, R. J., Décamps, H. & McClain, M. E. Riparia: ecology, conservation, and management of streamside communities (Elsevier Academic Press, 2005).Bayliss, S. L. J., Mueller, L. O., Ware, I. M., Schweitzer, J. A. & Bailey, J. K. Plant genetic variation drives geographic differences in atmosphere–plant–ecosystem feedbacks. Plant-Environ. Interact. 1, 166–180 (2020).
    Google Scholar 
    Cooke, J. E. K. & Rood, S. B. Trees of the people: the growing science of poplars in Canada and worldwide. This commentary is one of a selection of papers published in the Special Issue on Poplar Research in Canada. Can. J. Bot. 85, 1103–1110 (2007).
    Google Scholar 
    Evans, L. M., Allan, G. J., Meneses, N., Max, T. L. & Whitham, T. G. Herbivore host- associated genetic differentiation depends on the scale of plant genetic variation examined. Evol. Ecol. 27, 65–81 (2013).
    Google Scholar 
    Evans, L. M. et al. Geographical barriers and climate influence demographic history in narrowleaf cottonwoods. Heredity 114, 387–396 (2015).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Hargreaves, A. L., Samis, K. E., Eckert, C. G., Schmitz, A. E. O. J. & Bronstein, E. J. L. Are Species’ Range Limits Simply Niche Limits Writ Large? A Review of Transplant Experiments beyond the Range. Am. Nat. 183, 157–173 (2014).PubMed 

    Google Scholar 
    Gotelli, N. J. & Stanton-Geddes, J. Climate change, genetic markers and species distribution modelling. J. Biogeogr. 42, 1577–1585 (2015).
    Google Scholar 
    Cushman, S. A. et al. Landscape genetic connectivity in a riparian foundation tree is jointly driven by climatic gradients and river networks. Ecol. Appl. 24, 1000–1014 (2014).PubMed 

    Google Scholar 
    Bothwell, H. M. et al. Conserving threatened riparian ecosystems in the American West: Precipitation gradients and river networks drive genetic connectivity and diversity in a foundation riparian tree (Populus angustifolia). Mol. Ecol. 26, 5114–5132 (2017).PubMed 

    Google Scholar 
    Jimenez-Valverde, A. Sample Size for the evaluation of presence-absence models. Ecol. Indic. 114, 106289 (2020).
    Google Scholar 
    Hamann, A., Wang, T., Spittlehouse, D. L. & Murdock, T. Q. A Comprehensive, High-Resolution Database of Historical and Projected Climate Surfaces for Western North America. Bull. Am. Meteorol. Soc. 94, 1307–1309 (2013).
    Google Scholar 
    Lucinda. M. et al. NHDPlus version 2: user guide (Horizon Systems Corporation, 2012).ESRI. ArcMap (ESRI, 2018).Bayliss, S. L. J., Papeş, M., Schweitzer, J. A. & Bailey, J. K. Aggregate population-level models informed by genetics predict more suitable habitat than traditional species-level model across the range of a widespread riparian tree. PLoS One. 17, e0274892 (2022).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Elith, J. & Leathwick, J. R. Species Distribution Models: Ecological Explanation and Prediction Across Space and Time. Annu. Rev. Ecol. Evol. Syst. 40, 677–697 (2009).
    Google Scholar 
    Franklin, J. Mapping species distributions: spatial inference and prediction (Cambridge University Press, 2009).Bates, D., Maechler, M., Bolker, B. & Walker, S. Fitting Linear Mixed-Effects Models Using lme4. J. Stat. Softw. 67, 1–48 (2015). (1).
    Google Scholar 
    Elith, J. et al. A statistical explanation of MaxEnt for ecologists. Divers. Distrib. 17, 43–57 (2011).
    Google Scholar 
    Elith, J. et al. Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29, 129–151 (2006).
    Google Scholar 
    Pearson, R. G., Raxworthy, C. J., Nakamura, M. & Townsend Peterson, A. Predicting species distributions from small numbers of occurrence records: a test case using cryptic geckos in Madagascar. J. Biogeogr. 34, 102–117 (2007).
    Google Scholar 
    Swets, J. A. Measuring the Accuracy of Diagnostic Systems. Science 240, 1285–1293 (1988).CAS 
    PubMed 

    Google Scholar 
    Engler, R. et al. 21st century climate change threatens mountain flora unequally across Europe. Glob. Change Biol. 17, 2330–2341 (2011).
    Google Scholar 
    Randin, C. F. et al. Climate change and plant distribution: local models predict high-elevation persistence. Glob. Change Biol. 15, 1557–1569 (2009).
    Google Scholar 
    Knutti, R., Masson, D. & Gettelman, A. Climate model genealogy: Generation CMIP5 and how we got there. Geophys. Res. Lett. 40, 1194–1199 (2013).
    Google Scholar 
    Mateo, R. G., Mokany, K. & Guisan, A. Biodiversity Models: What If Unsaturation Is the Rule? Trends Ecol. Evol. 32, 556–566 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    R. Core Team. R: a language and environment for statistical computing (R Foundation for Statistical Computing, 2020).Oksanen, J. et al. vegan: community ecology package (2020) http://CRAN.R-project.org/package=vegan. More

  • in

    Site-specific temporal variation of population dynamics in subalpine endemic plant species

    Theurillat, J.-P. & Guisan, A. Potential impact of climate change on vegetation in the European Alps: A review. Clim. Change 50, 77–109 (2001).CAS 

    Google Scholar 
    Diaz, H. F. & Eischeid, J. K. Disappearing “alpine tundra” Köppen climatic type in the western United States. Geophys. Res. Lett. 34, L18707 (2007).ADS 

    Google Scholar 
    Dirnböck, T., Essl, F. & Rabitsch, W. Disproportional risk for habitat loss of high-altitude endemic species under climate change. Glob. Change Biol. 17, 990–996 (2011).ADS 

    Google Scholar 
    Myers, N., Mittermeier, R. A., Mittermeier, C. G., Da Fonseca, G. A. & Kent, J. Biodiversity hotspots for conservation priorities. Nature 403, 853–858 (2000).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Pauli, H., Gottfried, M., Dirnböck, T., Dullinger, S. & Grabherr, G. Assessing the long-term dynamics of endemic plants at summit habitats. In Alpine Biodiversity in Europe (eds. Nagy, L., Grabherr, G., Körner, C., & Thompson, D. B.) 195–207 (Springer, 2003).Cogoni, D., Sulis, E., Bacchetta, G. & Fenu, G. The unpredictable fate of the single population of a threatened narrow endemic Mediterranean plant. Biodivers. Conserv. 28, 1799–1813 (2019).
    Google Scholar 
    Cursach, J., Besnard, A., Rita, J. & Fréville, H. Demographic variation and conservation of the narrow endemic plant Ranunculus weyleri. Acta Oecol. 53, 102–109 (2013).ADS 

    Google Scholar 
    Dibner, R. R., DeMarche, M. L., Louthan, A. M. & Doak, D. F. Multiple mechanisms confer stability to isolated populations of a rare endemic plant. Ecol. Monogr. 89, e01360 (2019).
    Google Scholar 
    Boyce, M. S., Haridas, C. V., Lee, C. T., NCEAS Stochastic Demography Working Group. Demography in an increasingly variable world. Trends Ecol. Evol. 21, 141–148 (2006).PubMed 

    Google Scholar 
    Buckley, Y. M. et al. Causes and consequences of variation in plant population growth rate: A synthesis of matrix population models in a phylogenetic context. Ecol. Lett. 13, 1182–1197 (2010).PubMed 

    Google Scholar 
    Abbott, R. E., Doak, D. F. & DeMarche, M. L. Portfolio effects, climate change, and the persistence of small populations: Analyses on the rare plant Saussurea weberi. Ecology 98, 1071–1081 (2017).PubMed 

    Google Scholar 
    Villellas, J., Doak, D. F., García, M. B. & Morris, W. F. Demographic compensation among populations: What is it, how does it arise and what are its implications?. Ecol. Lett. 18, 1139–1152 (2015).PubMed 

    Google Scholar 
    Doak, D. F. & Morris, W. F. Demographic compensation and tipping points in climate-induced range shifts. Nature 467, 959–962 (2010).ADS 
    CAS 
    PubMed 

    Google Scholar 
    García-Camacho, R., Albert, M. J. & Escudero, A. Small-scale demographic compensation in a high-mountain endemic: The low edge stands still. Plant Ecol. Divers. 5, 37–44 (2012).
    Google Scholar 
    Andrello, M. et al. Accounting for stochasticity in demographic compensation along the elevational range of an alpine plant. Ecol. Lett. 23, 870–880 (2020).PubMed 

    Google Scholar 
    Valladares, F. et al. The effects of phenotypic plasticity and local adaptation on forecasts of species range shifts under climate change. Ecol. Lett. 17, 1351–1364 (2014).PubMed 

    Google Scholar 
    Ægisdóttir, H. H., Kuss, P. & Stöcklin, J. Isolated populations of a rare alpine plant show high genetic diversity and considerable population differentiation. Ann. Bot. 104, 1313–1322 (2009).PubMed 
    PubMed Central 

    Google Scholar 
    Morente-López, J. et al. Geography and environment shape landscape genetics of Mediterranean alpine species Silene ciliata Poiret. (Caryophyllaceae). Front. Plant Sci. 9, 1698 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    Franks, S. J., Weber, J. J. & Aitken, S. N. Evolutionary and plastic responses to climate change in terrestrial plant populations. Evol. Appl. 7, 123–139 (2014).PubMed 

    Google Scholar 
    Jeong, H., Cho, Y.-C. & Kim, E. Differential plastic responses to temperature and nitrogen deposition in the subalpine plant species, Primula farinosa subsp. modesta. AoB Plants 13, plab061 (2021).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Sulis, E., Bacchetta, G., Cogoni, D. & Fenu, G. From global to local scale: Where is the best for conservation purpose?. Biodivers. Conserv. 30, 183–200 (2021).
    Google Scholar 
    Hambler, D. & Dixon, J. Primula farinosa L. J. Ecol. 91, 694–705 (2003).
    Google Scholar 
    Arnold, E. & Richards, A. On the occurrence of unilateral incompatibility in Primula section Aleuritia Duby and the origin of Primula scotica Hook. Bot. J. Linn. Soc. 128, 359–368 (1998).
    Google Scholar 
    Tribsch, A. Areas of endemism of vascular plants in the eastern Alps in relation to Pleistocene glaciation. J. Biogeogr. 31, 747–760 (2004).
    Google Scholar 
    Chung, J.-M., Son, S.-W., Kim, S.-Y., Park, G.-W. & Kim, S.-S. Genetic diversity and geographic differentiation in the endangered Primula farinosa subsp. modesta, a subalpine endemic to Korea. Korean J. Plant. Taxon. 43, 236–243 (2013).
    Google Scholar 
    Lindborg, R. & Ehrlén, J. Evaluating the extinction risk of a perennial herb: Demographic data versus historical records. Conserv. Biol. 16, 683–690 (2002).
    Google Scholar 
    Caswell, H. Matrix Population Models, 2nd ed (Sinauer Associates Inc, 2000).Salguero-Gómez, R. & De Kroon, H. Matrix projection models meet variation in the real world. J. Ecol. 98, 250–254 (2010).
    Google Scholar 
    Jongejans, E. et al. Region versus site variation in the population dynamics of three short-lived perennials. J. Ecol. 98, 279–289 (2010).
    Google Scholar 
    Jongejans, E. & De Kroon, H. Space versus time variation in the population dynamics of three co-occurring perennial herbs. J. Ecol. 93, 681–692 (2005).
    Google Scholar 
    Suggitt, A. J. et al. Habitat microclimates drive fine-scale variation in extreme temperatures. Oikos 120, 1–8 (2011).
    Google Scholar 
    Tomimatsu, H. & Ohara, M. Demographic response of plant populations to habitat fragmentation and temporal environmental variability. Oecologia 162, 903–911 (2010).ADS 
    PubMed 

    Google Scholar 
    Kudernatsch, T., Fischer, A., Bernhardt-Römermann, M. & Abs, C. Short-term effects of temperature enhancement on growth and reproduction of alpine grassland species. Basic Appl. Ecol. 9, 263–274 (2008).
    Google Scholar 
    Kim, E. & Donohue, K. Local adaptation and plasticity of Erysimum capitatum to altitude: Its implications for responses to climate change. J. Ecol. 101, 796–805 (2013).
    Google Scholar 
    Forbis, T. A. Seedling demography in an alpine ecosystem. Am. J. Bot. 90, 1197–1206 (2003).PubMed 

    Google Scholar 
    Yenni, G., Adler, P. B. & Ernest, S. M. Strong self-limitation promotes the persistence of rare species. Ecology 93, 456–461 (2012).PubMed 

    Google Scholar 
    Doak, D. F. Source-sink models and the problem of habitat degradation: General models and applications to the Yellowstone grizzly. Conserv. Biol. 9, 1370–1379 (1995).
    Google Scholar 
    Lesica, P. & Crone, E. E. Arctic and boreal plant species decline at their southern range limits in the Rocky Mountains. Ecol. Lett. 20, 166–174 (2017).PubMed 

    Google Scholar 
    Oldfather, M. F. & Ackerly, D. D. Microclimate and demography interact to shape stable population dynamics across the range of an alpine plant. New Phytol. 222, 193–205 (2019).PubMed 

    Google Scholar 
    Ågren, J., Fortunel, C. & Ehrlén, J. Selection on floral display in insect-pollinated Primula farinosa: Effects of vegetation height and litter accumulation. Oecologia 150, 225–232 (2006).ADS 
    PubMed 

    Google Scholar 
    Ehrlén, J., Syrjänen, K., Leimu, R., Begona Garcia, M. & Lehtilä, K. Land use and population growth of Primula veris: An experimental demographic approach. J. Appl. Ecol. 42, 317–326 (2005).
    Google Scholar 
    Ehrlén, J. & Morris, W. F. Predicting changes in the distribution and abundance of species under environmental change. Ecol. Lett. 18, 303–314 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    Stubben, C. & Milligan, B. Estimating and analyzing demographic models using the popbio package in R. J. Stat. Softw. 22, 1–23 (2007).
    Google Scholar 
    Weiss, N. Package ‘wPerm’. https://cran.r-project.org/web/packages/wPerm/wPerm.pdf. (2015).Frossard, J. & Renaud, O. Permutation tests for regression, ANOVA, and comparison of signals: The permuco package. J. Stat. Softw. 99, 1–32 (2021).
    Google Scholar  More