Philippa Kaur

1.Norris, K. S. & Dohl, T. P. The Structure and Functions of Cetacean Schools (1979).2.Frantzis, A. & Herzing, D. L. Mixed-species associations of striped dolphins (Stenella coeruleoalba), short-beaked common dolphins (Delphinus delphis), and Risso’s dolphins (Grampus griseus) in the Gulf of Corinth (Greece, Mediterranean Sea).” Aquatic Mammals 28.2 (2002): 188–197.3.Crossman, C., Barrett-Lennard, L. & Taylor, E. Population structure and intergeneric hybridization in harbour porpoises Phocoena phocoena in British Columbia, Canada. Endang. Species. Res. 26, 1–12 (2014).Article 

Google Scholar 
4.Espada, R., Olaya-Ponzone, L., Haasova, L., Martín, E. & García-Gómez, J. C. Hybridization in the wild between Tursiops truncatus (Montagu 1821) and Delphinus delphis (Linnaeus 1758). PLoS ONE 14, e0215020 (2019).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
5.Herzing, D. L., Moewe, K. & Brunnick, B. J. Interspecies interactions between Atlantic spotted dolphins, Stenella frontalis and bottlenose dolphins, Tursiops truncatus, on Great Bahama Bank Bahamas. Aquat. Mamm. 29, 335–341 (2003).Article 

Google Scholar 
6.Herzing, D. L. Vocalizations and associated underwater behavior of free-ranging Atlantic spotted dolphins, Stenella frontalis and bottlenose dolphins, Tursiops truncatus. Aquat. Mamm. 22, 61–80 (1996).
Google Scholar 
7.Herzing, D. L. & Johnson, C. M. Interspecific interactions between Atlantic spotted dolphins (Stenella frontalis) and bottlenose dolphins (Tursiops truncatus) in the Bahamas 1985–1995. Aquat. Mamm. 23, 85–99 (1997).
Google Scholar 
8.Orr, J. R. & Harwood, L. A. Possible aggressive behavior between a narwhal (Monodon monoceros) and a beluga (Delphinapterus leucas). Mar. Mamm. Sci. 14, 182–185 (1998).Article 

Google Scholar 
9.Puig-Lozano, R. et al. Retrospective study of traumatic intra-interspecific interactions in stranded cetaceans, Canary Islands. Front. Vet. Sci. 7, 107 (2020).PubMed 
PubMed Central 
Article 

Google Scholar 
10.Shane, S. Relationship between pilot whales and Risso’s dolphins at Santa Catalina Island, California, USA. Mar. Ecol. Prog. Ser. 123, 5–11 (1995).ADS 
Article 

Google Scholar 
11.Haelters, J. & Everaarts, E. Two cases of physical interaction between white-beaked dolphins (Lagenorhynchus albirostris) and juvenile harbour porpoises (Phocoena phocoena) in the southern North Sea. Aquat. Mamm. 37, 198 (2011).Article 

Google Scholar 
12.Jepson, P. D. & Baker, J. R. Bottlenosed dolphins (Tursiops truncatus) as a possible cause of acute traumatic injuries in porpoises (Phocoena phocoena). Vet. Rec. 143, 614–615 (1998).CAS 
PubMed 
Article 

Google Scholar 
13.Patterson, I. A. P., Reid, R. J., Wilson, B., Grellier, K. & Ross, H. M. Evidence for infanticide in bottlenose dolphins: An explanation for violent interactions with harbour porpoises?. Proc. R. Soc. Lond. Ser. B Biol. Sci. 265, 1167–1170 (1998).CAS 
Article 

Google Scholar 
14.Ross, H. M. & Wilson, B. Violent interactions between bottlenose dolphins and harbour porpoises. Proc. R. Soc. Lond. Ser. B Biol. Sci. 263, 283–286 (1996).ADS 
Article 

Google Scholar 
15.Wilson, B., Reid, R. J., Grellier, K., Thompson, P. M. & Hammond, P. S. Considering the temporal when managing the spatial: A population range expansion impacts protected areas-based management for bottlenose dolphins. Anim. Conserv. 7, 331–338 (2004).Article 

Google Scholar 
16.Alonso, J. M., López, A., González, A. F. & Santos, M. B. Evidence of violent interactions between bottlenose dolphin (Tursiops truncatus) and other cetacean species in NW Spain. In Proceedings of the 14th Annual Conference of The European Cetacean Society (2000).17.López, A. & Rodriguez, A. Agresion de arroas (Tursiops truncatus) a toniña (Phocoena phocoena). Eubalaena 6, 23–27 (1995).
Google Scholar 
18.Methion, S. & Díaz López, B. Spatial segregation and interspecific killing of common dolphins (Delphinus delphis) by bottlenose dolphins (Tursiops truncatus). Acta Ethol. 24, 95–106 (2021).Article 

Google Scholar 
19.Parsons, K. M., Durban, J. W. & Claridge, D. E. Male-male aggression renders bottlenose dolphin (Tursiops truncatus) unconscious. Aquat. Mamm. 29, 360–362 (2003).Article 

Google Scholar 
20.Robinson, K. P. Agonistic intraspecific behavior in free-ranging bottlenose dolphins: Calf-directed aggression and infanticidal tendencies by adult males. Mar. Mamm. Sci. 30, 381–388 (2014).Article 

Google Scholar 
21.Scott, E. M., Mann, J., Watson-Capps, J. J., Sargeant, B. L., & Connor, R. C. Aggression in bottlenose
dolphins: evidence for sexual coercion, male-male competition, and female tolerance through analysis of tooth-rake
marks and behaviour. Behaviour 21–44 (2005).22.Díaz López, B., López, A., Methion, S. & Covelo, P. Infanticide attacks and associated epimeletic behaviour in free-ranging common bottlenose dolphins (Tursiops truncatus). J. Mar. Biol. Assoc. 98, 1159–1167 (2018).Article 

Google Scholar 
23.Cotter, M. P., Maldini, D. & Jefferson, T. A. “Porpicide” in California: Killing of harbor porpoises (Phocoena phocoena) by coastal bottlenose dolphins (Tursiops truncatus). Mar. Mamm. Sci. 28, E1–E15 (2012).Article 

Google Scholar 
24.Forney, K. A. Environmental models of cetacean abundance: Reducing uncertainty in population trends. Conserv. Biol. 14, 1271–1286 (2000).Article 

Google Scholar 
25.Gowans, S., Würsig, B. & Karczmarski, L. The social structure and strategies of delphinids: predictions based on an ecological framework. In Advances in Marine Biology Vol. 53, 195–294 (Elsevier, 2007).26.Miller, E. H. Territorial behavior. In Encyclopedia of marine mammals 1156–1166 (Academic Press, 2009).27.Díaz López, B. Bottlenose dolphins and aquaculture: Interaction and site fidelity on the north-eastern coast of Sardinia (Italy). Mar. Biol. 159, 2161–2172 (2012).Article 

Google Scholar 
28.Bearzi, G., Piwetz, S. & Reeves, R. R. Odontocete adaptations to human impact and vice versa. In Ethology and Behavioral Ecology of Odontocetes (ed. Würsig, B.) 211–235 (Springer International Publishing, 2019) https://doi.org/10.1007/978-3-030-16663-2_10.Chapter 

Google Scholar 
29.Bonizzoni, S. et al. Fish farming and its appeal to common bottlenose dolphins: Modelling habitat use in a Mediterranean embayment: Fish farming appeal to bottlenose dolphins. Aquatic Conserv. Mar. Freshw. Ecosyst. 24, 696–711 (2014).Article 

Google Scholar 
30.Díaz López, B. Bottlenose dolphin (Tursiops truncatus) predation on a marine fin fish farm: Some underwater observations. Aquat. Mamm. 32, 305–310 (2006).Article 

Google Scholar 
31.Díaz López, B., Marini, L. & Polo, F. The impact of a fish farm on a bottlenose dolphin population in the Mediterranean Sea. Thalassas 21, 65–70 (2005).
Google Scholar 
32.Piroddi, C., Bearzi, G. & Christensen, V. Marine open cage aquaculture in the eastern Mediterranean Sea: A new trophic resource for bottlenose dolphins. Mar. Ecol. Prog. Ser. 440, 255–266 (2011).ADS 
Article 

Google Scholar 
33.Díaz López, B. The bottlenose dolphin Tursiops truncatus foraging around a fish farm: Effects of prey abundance on dolphins’ behavior. Curr. Zool. 55, 243–248 (2009).Article 

Google Scholar 
34.Castellote, M., Brotons, J. M., Chicote, C., Gazo, M. & Cerdà, M. Long-term acoustic monitoring of bottlenose dolphins, Tursiops truncatus, in marine protected areas in the Spanish Mediterranean Sea. Ocean Coast. Manag. 113, 54–66 (2015).Article 

Google Scholar 
35.Aznar, F. et al. Long-term changes (1990–2012) in the diet of striped dolphins Stenella coeruleoalba from the western Mediterranean. Mar. Ecol. Prog. Ser. 568, 231–247 (2017).ADS 
Article 

Google Scholar 
36.Calzada, N., Aguilar, A., Grau, E. & Lockyer, C. Patterns of growth and physical maturity in the western Mediterranean striped dolphin, Stenella coeruleoalba (Cetacea: Odontoceti). Can. J. Zool. 75, 632–637 (1997).Article 

Google Scholar 
37.Meissner, A. M., MacLeod, C. D., Richard, P., Ridoux, V. & Pierce, G. Feeding ecology of striped dolphins, Stenella coeruleoalba, in the north-western Mediterranean Sea based on stable isotope analyses. J. Mar. Biol. Assoc. 92, 1677–1687 (2012).CAS 
Article 

Google Scholar 
38.Chen, I., Watson, A. & Chou, L.-S. Insights from life history traits of Risso’s dolphins (Grampus griseus) in Taiwanese waters: Shorter body length characterizes northwest Pacific population. Mar. Mamm. Sci. 27, E43–E64 (2011).Article 

Google Scholar 
39.Barnett, J. et al. Postmortem evidence of interactions of bottlenose dolphins (Tursiops truncatus) with other dolphin species in south-west England. Vet. Rec. 165, 441–444 (2009).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
40.Townsend, F. I. & Staggs, L. Atlas of Skin Diseases of Small Cetaceans (Todd Speakman, 2020).
Google Scholar 
41.Jefferson, T. A., Stacey, P. J. & Baird, R. W. A review of Killer Whale interactions with other marine mammals: Predation to co-existence. Mamm. Rev. 21, 151–180 (1991).Article 

Google Scholar 
42.Weller, D. W. et al. Observations of an interaction between sperm whales and short-finned pilot whales in the Gulf of Mexico. Mar. Mamm. Sci. 12, 588–594 (1996).ADS 
Article 

Google Scholar 
43.Baird, R. W. An interaction between Pacific white-sided dolphins and a neonatal harbor porpoise. Mammalia 62, 129–133 (1998).
Google Scholar 
44.Wedekin, L. L., Daura-Jorge, F. G. & Simoes-Lopes, P. C. An aggressive interaction between bottlenose dolphins (Tursiops truncatus) and estuarine dolphins (Sotalia guianensis) in southern Brazil. Aquat. Mamm. 30, 391–397 (2004).Article 

Google Scholar 
45.Campbell-Malone, R. et al. Gross and histologic evidence of sharp and blunt trauma in north Atlantic right whales (Eubalaena glacialis) killed by vessels. J. Zoo Wildl. Med. 39, 37–55 (2008).PubMed 
Article 

Google Scholar 
46.Moore, M. et al. Criteria and case definitions for serious injury and death of pinnipeds and cetaceans caused by anthropogenic trauma. Dis. Aquat. Org. 103, 229–264 (2013).CAS 
Article 

Google Scholar 
47.Read, A. & Murray, K. Gross Evidence of Human-Induced Mortality in Small Cetaceans (2000).48.Gozalbes, P. et al. Cetáceos y tortugas marinas en la Comunitat Valenciana. 20 años de seguimiento (2010).49.Gómez de Segura, A., Hammond, P. S. & Raga, J. A. Influence of environmental factors on small cetacean distribution in the Spanish Mediterranean. J. Mar. Biol. Assoc. 88, 1185–1192 (2008).Article 

Google Scholar 
50.Cañadas, A., Sagarminaga, R., De Stephanis, R., Urquiola, E. & Hammond, P. S. Habitat preference modelling as a conservation tool: Proposals for marine protected areas for cetaceans in southern Spanish waters. Aquat. Conserv. Mar. Freshw. Ecosyst. 15, 495–521 (2005).Article 

Google Scholar 
51.Gannier, A. Diel variations of the striped dolphin distribution off the French Riviera (Northwestern Mediterranean Sea). Aquat. Mamm. 25, 123–134 (1999).
Google Scholar 
52.Blanco, C., Aznar, J. & Raga, J. A. Cephalopods in the diet of the striped dolphin Stenella coeruleoalba from the western Mediterranean during an epizootic in 1990. J. Zool. 237, 151–158 (1995).Article 

Google Scholar 
53.Archer II, F. I. Striped dolphin: Stenella coeruleoalba. In Encyclopedia of Marine Mammals 1127–1129 (Academic Press, 2009).54.Fraija-Fernández, N. et al. Long term boat-based surveys in the Central Spanish Mediterranean (2003–2013): Cetacean diversity and distribution. In Proceeding of the 29th Conference of the European Cetacean Society (2015).55.Blanco, C., Salomón, O. & Raga, J. A. Diet of the bottlenose dolphin (Tursiops truncatus) in the western Mediterranean Sea. J. Mar. Biol. Assoc. 81, 1053–1058 (2001).Article 

Google Scholar 
56.Praca, E. & Gannier, A. Ecological niches of three teuthophageous odontocetes in the northwestern Mediterranean Sea. Ocean Sci. 4, 49–59 (2008).ADS 
Article 

Google Scholar 
57.Bearzi, G., Fortuna, C. M. & Reeves, R. R. Ecology and conservation of common bottlenose dolphins Tursiops truncatus in the Mediterranean Sea. Mamm. Rev. 39, 92–123 (2009).Article 

Google Scholar 
58.Epperly, S. P. et al. Beach strandings as an indicator of at-sea mortality of sea turtles. Bull. Mar. Sci. 59(2), 289–297 (1996).
Google Scholar 
59.Peltier, H. et al. The significance of stranding data as indicators of cetacean populations at sea: Modelling the drift of cetacean carcasses. Ecol. Ind. 18, 278–290 (2012).Article 

Google Scholar 
60.Martínez-Cedeira, J. A. et al. How many strand? Offshore marking and coastal recapture of cetacean carcasses. In Abstract Book—25th Conference of the European Cetacean Society 332 (2011).61.Gulland, F. M., Dierauf, L. A. & Whitman, K. L. CRC Handbook of Marine Mammal medicine (CRC Press, 2018).
Google Scholar 
62.Isidoro-Ayza, M. et al. Brucella ceti infection in dolphins from the Western Mediterranean sea. BMC Vet. Res. 10, 206 (2014).PubMed 
PubMed Central 
Article 

Google Scholar 
63.Rubio-Guerri, C. et al. Unusual striped dolphin mass mortality episode related to cetacean morbillivirus in the Spanish Mediterranean sea. BMC Vet. Res. 9, 106 (2013).PubMed 
PubMed Central 
Article 

Google Scholar 
64.Kuiken, T. & Hartmann, M. G. Proceedings of the First ECS Workshop on Cetacean Pathology: Dissection Techniques and Tissue Sampling. Vol. 17 (1991).65.Geraci, J. R. & Lounsbury, V. J. Marine Mammals Ashore: A Field guide for Strandings (National Aquarium in Baltimore, 2005).
Google Scholar 
66.Pugliares, K. R. et al. Marine Mammal Necropsy: An Introductory Guide for Stranding Responders and Field Biologists (Woods Hole Oceanographic Institution, 2007) https://doi.org/10.1575/1912/1823.Book 

Google Scholar 
67.Long, D. J. & Jones, R. E. White shark predation and scavenging on cetaceans in the eastern North Pacific Ocean. In Great White Sharks: The Biology of Carcharodon carcharias 293–307 (1996).68.Rubio-Guerri, C. et al. Simultaneous diagnosis of Cetacean morbillivirus infection in dolphins stranded in the Spanish Mediterranean sea in 2011 using a novel Universal Probe Library (UPL) RT-PCR assay. Vet. Microbiol. 165, 109–114 (2013).PubMed 
Article 

Google Scholar 
69.Van Devanter, D. R. et al. Detection and analysis of diverse herpesviral species by consensus primer PCR. J. Clin. Microbiol. 34, 1666–1671 (1996).CAS 
Article 

Google Scholar 
70.Alton, G. G., Jones, L. M., Angus, R. D. & Verger, J. M. Techniques for the Brucellosis Laboratory (Institut National de la Recherche Agronomique (INRA), 1988).
Google Scholar  More

1.Schäferna, K. Amphipoda balcanica, spolu s poznámkami o jiných sladkovodních Amphipodech. Mem. Soc. R. Sci. Boheme Prague 12, 1–111 (1922).
Google Scholar 
2.Martynov, A. B. Zur Kenntnis der Amphipoden der Krim. Zool. Jahrb. 60, 573–606 (1931).
Google Scholar 
3.Karaman, S. L. Beitrag zur Kenntni s der Susswasseramphiopden. Bull. Soc. Scien Skoplje IX, 93–107 (1931).
Google Scholar 
4.Schellenberg, A. Schlussel und Diagnosen der dem Susswasser-Gammarus nahestehenden Einheiten ausschlisslich der Arten des Baikalsees und Australiens. Zool. Anz. 117, 267–280 (1937).
Google Scholar 
5.Barnard, J. L. & Karaman, S. G. Classificatory revisions in gammaridean amphipoda (Crustacea), Part 2. Proc. Biol. Soc. Wash. 95, 167–187 (1982).
Google Scholar 
6.Karaman, G. & Pinkster, S. Freshwater Gammarus species from Europe, North Africa and adjacent regions of Asia (CrustaceaAmphipoda): Part I: Gammarus pulex-group and related species. Bijdr Dierkd 47, 1–97 (1977).Article 

Google Scholar 
7.Karaman, G. & Pinkster, S. Freshwater Gammarus species from Europe, North Africa and adjacent regions of Asia (Crustacea Amphipoda): Part II: Gammarus roeseli-group and related species. Bijdr Dierkd 47, 165–196 (1977).Article 

Google Scholar 
8.Karaman, G. & Pinkster, S. Freshwater Gammarus species from Europe, North Africa and adjacent regions of Asia (Crustacea-Amphipoda): Part III: Gammarus balcanicus-group and related species. Bijdr Dierkd 57, 207–260 (1987).Article 

Google Scholar 
9.Jażdżewski, K. Remarks on Gammarus lacustris G.O. Sars, 1863, with description of Gammarus varsoviensis n. sp. Bijdr Dierkd 45, 71–86 (1975).Article 

Google Scholar 
10.Jażdżewski, K. & Konopacka, A. Gammarus leopoliensis nov. sp. (Crustacea, Amphipoda) from Eastern Carpathians. Bull. Zoölogisch Museum 11, 185–196 (1989).
Google Scholar 
11.Karaman, G. S. New species of the family Gammaridae from Ohrid Lake basin, Gammarus sketi, n. sp., with emphasis on the subterranean members of genus Gammarus Fabr. (Contribution to the knowledge of the Amphipoda 191). Glasnik Odjeljenja prirodnih nauka, Crnogorska akademija nauka i umjetnosti 7, 53–71 (1989).
Google Scholar 
12.Iannilli, V. & Ruffo, S. Apennine and Sardinian species of Gammarus, with the description of Gammarus elvirae n. sp. (Crustacea Amphipoda, Gammaridae). Boll. Acc. Gioenia Sci. Nat 35, 519–532 (2002).
Google Scholar 
13.Alther, R., Fišer, C. & Altermatt, F. Description of a widely distributed but overlooked amphipod species in the European Alps. Zool. J. Linn Soc.-Lond. https://doi.org/10.1111/zoj.12477 (2016).Article 

Google Scholar 
14.Grabowski, M., Wysocka, A. & Mamos, T. Molecular species delimitation methods provide new insight into taxonomy of the endemic gammarid species flock from the ancient Lake Ohrid. Zool. J. Linn. Soc.-Lond. 20, 1–14. https://doi.org/10.1093/zoolinnean/zlw025 (2017).Article 

Google Scholar 
15.Hupalo, K., Mamos, T., Wrzesinska, W. & Grabowski, M. First endemic freshwater Gammarus from Crete and its evolutionary history-an integrative taxonomy approach. PeerJ 6, e4457. https://doi.org/10.7717/peerj.4457 (2018).Article 
PubMed 
PubMed Central 

Google Scholar 
16.Rudolph, K., Coleman, C. O., Mamos, T. & Grabowski, M. Description and post-glacial demography of Gammarus jazdzewskii sp. Nov. (Crustacea: Amphipoda) from Central Europe. Syst. Biodivers. 16, 587–603. https://doi.org/10.1080/14772000.2018.1470118 (2018).Article 

Google Scholar 
17.Hou, Z., Sket, B. & Li, S. Phylogenetic analyses of Gammaridae crustacean reveal different diversification patterns among sister lineages in the Tethyan region. Cladistics https://doi.org/10.1111/cla.12055 (2014).Article 

Google Scholar 
18.Hou, Z. & Sket, B. A review of Gammaridae (Crustacea: Amphipoda): The family extent, its evolutionary history, and taxonomic redefinition of genera. Zool. J. Linn. Soc.-Lond. 176, 323–348. https://doi.org/10.1111/zoj.12318 (2016).Article 

Google Scholar 
19.Sket, B. & Hou, Z. Family Gammaridae (Crustacea: Amphipoda), mainly its Echinogammarus clade in SW Europe. Further elucidation of its phylogeny and taxonomy. ABS 61 (2018).20.Mamos, T., Wattier, R., Burzyński, A. & Grabowski, M. The legacy of a vanished sea: A high level of diversification within a European freshwater amphipod species complex driven by 15 My of Paratethys regression. Mol. Ecol. 25, 795–810. https://doi.org/10.1111/mec.13499 (2016).Article 
PubMed 

Google Scholar 
21.Mamos, T., Wattier, R., Majda, A., Sket, B. & Grabowski, M. Morphological vs. molecular delineation of taxa across montane regions in Europe: The case study of Gammarus balcanicus Schäferna, 1922 (Crustacea: Amphipoda). J. Zoolog. Syst. Evol. Res. 52, 237–248. https://doi.org/10.1111/jzs.12062 (2014).Article 

Google Scholar 
22.Grabowski, M., Mamos, T., Bącela-Spychalska, K., Rewicz, T. & Wattier, R. A. Neogene paleogeography provides context for understanding the origin and spatial distribution of cryptic diversity in a widespread Balkan freshwater amphipod. PeerJ 5, e3016. https://doi.org/10.7717/peerj.3016 (2017).Article 
PubMed 
PubMed Central 

Google Scholar 
23.Copilaş-Ciocianu, D., Zimţa, A.-A., Grabowski, M. & Petrusek, A. Survival in northern microrefugia in an endemic Carpathian gammarid (Crustacea: Amphipoda). Zool. Scr. 47, 357–372. https://doi.org/10.1111/zsc.12285 (2018).Article 

Google Scholar 
24.Copilaş-Ciocianu, D. & Petrusek, A. Phylogeography of a freshwater crustacean species complex reflects a long-gone archipelago. J. Biogeogr. 44, 421–432. https://doi.org/10.1111/jbi.12853 (2017).Article 

Google Scholar 
25.Wattier, R. et al. Continental-scale patterns of hyper-cryptic diversity within the freshwater model taxon Gammarus fossarum (Crustacea, Amphipoda). Sci. Rep. 10, 16536. https://doi.org/10.1038/s41598-020-73739-0 (2020).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
26.Meier, R. & Wheeler, Q. D. in The New Taxonomy (ed Q. D. Wheeler) 256 (CRC Press, 2008).27.Coleman, C. O. Taxonomy in times of the taxonomic impediment: Examples from the community of experts on amphipod crustaceans. J. Crustacean Biol. 35, 729–740. https://doi.org/10.1163/1937240x-00002381 (2015).Article 

Google Scholar 
28.Puillandre, N., Brouillet, S. & Achaz, G. ASAP: Assemble species by automatic partitioning. Mol. Ecol. Resour. 21, 609–620. https://doi.org/10.1111/1755-0998.13281 (2021).Article 
PubMed 

Google Scholar 
29.Kondracki, J. Karpaty. (WSiP, 1989).30.Mráz, P. & Ronikier, M. Biogeography of the Carpathians: Evolutionary and spatial facets of biodiversity. Biol. J. Linn. Soc. 119, 528–559. https://doi.org/10.1111/bij.12918 (2016).Article 

Google Scholar 
31.Balint, M. et al. Biodiversity Hotspots: Distribution and Protection of Conservation Priority Areas 189–205 (Springer, 2011).Book 

Google Scholar 
32.Schmitt, T. & Varga, Z. Extra-Mediterranean refugia: The rule and not the exception?. Front Zool. https://doi.org/10.1186/1742-9994-9-22 (2012).Article 
PubMed 
PubMed Central 

Google Scholar 
33.Ronikier, M. Biogeography of high-mountain plants in the Carpathians: An emerging phylogeographical perspective. Taxon 60, 373–389. https://doi.org/10.1002/tax.602008 (2011).Article 

Google Scholar 
34.Hájková, P. et al. Using multi-proxy palaeoecology to test a relict status of refugial populations of calcareous-fen species in the Western Carpathians. The Holocene 25, 702–715. https://doi.org/10.1177/0959683614566251 (2015).ADS 
Article 

Google Scholar 
35.Malicky, H. Chorological patterns and biome types of European Trichoptera and other freshwater insects. Arch. Hydrobiol. 96, 223–244 (1983).
Google Scholar 
36.Malicky, H. Arealdynamik und Biomgrundtypen am Beispiel der Köcherfliegen (Trichoptera). Entom Basi 22, 235–259 (2000).
Google Scholar 
37.Keresztes, L., Kolcsár, L.-P., Török, E. & Dénes, A.-L. in The Carpathians as speciation centres and barriers: From case studies to general patterns (eds L Keresztes & B. Markó) 168 (Cluj University Press, 2011).38.Bozáová, J., Čiamporová Zat’ovičová, Z., Čiampor, F., Mamos, T. & Grabowski, M. The tale of springs and streams: How different aquatic ecosystems impacted the mtDNA population structure of two riffle beetles in the Western Carpathians. PeerJ 8, e10039. https://doi.org/10.7717/peerj.10039 (2020).Article 

Google Scholar 
39.Copilas-Ciocianu, D., Rutová, T., Pařil, P. & Petrusek, A. Epigean gammarids survived millions of years of severe climatic fluctuations in high latitude refugia throughout the Western Carpathians. Mol. Phylogenet. Evol. 112, 218–229. https://doi.org/10.1016/j.ympev.2017.04.027 (2017).Article 
PubMed 

Google Scholar 
40.Grabowski, M. & Mamos, T. Contact Zones, Range Boundaries, and Vertical Distribution of Three Epigean Gammarids (Amphipoda) in the Sudeten and Carpathian Mountains (Poland). Crustaceana 84, 153–168. https://doi.org/10.1163/001121611×554328 (2011).Article 

Google Scholar 
41.Jażdżewski, K. Morfologia, taksonomia i występowanie w Polsce kiełży z rodzajów Gammarus Fabr. i Chaetogammarus Mart. (Crustacea, Amphipoda). 185 (Acta Universitatis Lodziensis, 1975).42.Jażdżewski, K. & Konopacka, A. Notes on the Gammaridean Amphipoda of the Dniester River Basin and Eastern Carpathians. Crustaceana. Supplement, 72–89 (1988).43.Zieliński, D. Life History of Gammarus balcanicus Schäferna, 1922 from the Bieszczady Mountains (Eastern Carpathians, Poland). Crustaceana 68(1), 61–72 (1995).Article 

Google Scholar 
44.Zieliński, D. Life Cycle and Altitude Range of Gammarus leopoliensis Jażdżewski & Konopacka, 1989 (Amphipoda) in South-Eastern Poland. Crustaceana 71 (1998).45.Konopacka A., Jażdżewski K., Jędryczkowski W. In Monografie Bieszczadzkie, vol. VII (ed. Pawłowski, J.) (2000).46.Straškraba, M. Předběžná zpráva o rozšíření rodu Gammarus v ČSR. Věstník Československé Společnosti Zoologické 17, 212–227 (1953).
Google Scholar 
47.Straškraba, M. Beitrag zur Kenntnis der Amphipodenfauna Karpatenrusslands (USSR). Věstník Československé Společnosti Zoologické 21, 256–272 (1957).
Google Scholar 
48.Micherdziński, W. Kiełże rodzaju Gammarus Fabricius (Amphipoda) w wodach Polski. Acta Zoologica Cracoviensia 4, 527–637 (1959).
Google Scholar 
49.Straškraba, M. Amphipoden der Tschechoslovakei nach den Sammlungen von. Prof. Hrabě. I. Věstník Československé Společnosti Zoologické 26, 117–145 (1962).50.Provan, J. & Bennett, K. D. Phylogeographic insights into cryptic glacial refugia. Trends Ecol. Evol. 23, 564–571. https://doi.org/10.1016/j.tree.2008.06.010 (2008).Article 
PubMed 

Google Scholar 
51.Tzedakis, P. C., Emerson, B. C. & Hewitt, G. M. Cryptic or mystic? Glacial tree refugia in northern Europe. Trends Ecol. Evol. 28, 696–704. https://doi.org/10.1016/j.tree.2013.09.001 (2013).CAS 
Article 
PubMed 

Google Scholar 
52.Harl, J., Duda, M., Kruckenhauser, L., Sattmann, H. & Haring, E. In Search of Glacial Refuges of the Land Snail Orcula dolium (Pulmonata, Orculidae): An Integrative Approach Using DNA Sequence and Fossil Data. PLoS ONE 9, e96012. https://doi.org/10.1371/journal.pone.0096012 (2014).ADS 
CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
53.Juřičková, L., Horáčková, J. & Ložek, V. Direct evidence of central European forest refugia during the last glacial period based on mollusc fossils. Quaternary Res. 82, 222–228. https://doi.org/10.1016/j.yqres.2014.01.015 (2014).ADS 
Article 

Google Scholar 
54.Väinölä, R. et al. Global diversity of amphipods (Amphipoda; Crustacea) in freshwater. Hydrobiologia 595, 241–255. https://doi.org/10.1007/s10750-007-9020-6 (2008).Article 

Google Scholar 
55.Zasadni, J. & Kłapyta, P. The tatra mountains during the last glacial maximum. J. Maps 10, 440–456. https://doi.org/10.1080/17445647.2014.885854 (2014).Article 

Google Scholar 
56.Sworobowicz, L., Mamos, T., Grabowski, M. & Wysocka, A. Lasting through the ice age: The role of the proglacial refugia in the maintenance of genetic diversity, population growth, and high dispersal rate in a widespread freshwater crustacean. Freshwater Biol. 65, 1028–1046. https://doi.org/10.1111/fwb.13487 (2020).CAS 
Article 

Google Scholar 
57.Ratnasingham, S. & Hebert, P. Bold: The barcode of life data system. Mol. Ecol. Not. 7, 355–364. https://doi.org/10.1111/j.1471-8286.2007.01678.x (2007).CAS 
Article 

Google Scholar 
58.Weigand, H. et al. DNA barcode reference libraries for the monitoring of aquatic biota in Europe: Gap-analysis and recommendations for future work. STOTEN 678, 499–524. https://doi.org/10.1016/j.scitotenv.2019.04.247 (2019).ADS 
CAS 
Article 

Google Scholar 
59.Katouzian, A.-R. et al. Drastic underestimation of amphipod biodiversity in the endangered Irano-Anatolian and Caucasus biodiversity hotspots. Sci. Rep. 6, 22507. https://doi.org/10.1038/srep22507 (2016).ADS 
CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
60.Bickford, D. et al. Cryptic species as a window on diversity and conservation. Trends Ecol. Evol. 22, 148–155. https://doi.org/10.1016/j.tree.2006.11.004 (2007).Article 
PubMed 

Google Scholar 
61.Delić, T., Trontelj, P., Rendoš, M. & Fišer, C. The importance of naming cryptic species and the conservation of endemic subterranean amphipods. Sci. Rep. 7, 3391. https://doi.org/10.1038/s41598-017-02938-z (2017).ADS 
CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
62.Maddison, W. P. Gene trees in species trees. Syst. Biol. 46, 523–536. https://doi.org/10.2307/2413694 (1997).Article 

Google Scholar 
63.Nosil, P. Speciation with gene flow could be common. Mol. Ecol. 17, 2103–2106. https://doi.org/10.1111/j.1365-294X.2008.03715.x (2008).Article 
PubMed 

Google Scholar 
64.Berner, D. & Salzburger, W. The genomics of organismal diversification illuminated by adaptive radiations. Trends Genet. 31, 491–499. https://doi.org/10.1016/j.tig.2015.07.002 (2015).CAS 
Article 
PubMed 

Google Scholar 
65.Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. .Biol 215, 403–410. https://doi.org/10.1006/jmbi.1990.9999 (1990).CAS 
Article 
PubMed 

Google Scholar 
66.Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. https://doi.org/10.1093/molbev/mst010 (2013).Article 
PubMed 
PubMed Central 

Google Scholar 
67.Xia, X. DAMBE5: A comprehensive software package for data analysis. Mol. Biol. Evol. 30, 1720–1728. https://doi.org/10.1093/molbev/mst064 (2013).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
68.Xia, X., Xie, Z., Salemi, M., Chen, L. & Wang, Y. An index of substitution saturation and its application. Mol. Phylogenet. Evol. 26, 1–7. https://doi.org/10.1016/S1055-7903(02)00326-3 (2003).CAS 
Article 
PubMed 

Google Scholar 
69.Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547–1549. https://doi.org/10.1093/molbev/msy096 (2018).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
70.Saitou, N. & Nei, M. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454 (1987).CAS 
Article 
PubMed 

Google Scholar 
71.Kimura, M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. https://doi.org/10.1007/bf01731581 (1980).Article 
PubMed 

Google Scholar 
72.Felsenstein, J. Confidence limits on phylogenies: An approach using the bootstrap. Evol. Int. J. Org. Evol. 39, 783–791 (1985).Article 

Google Scholar 
73.Ratnasingham, S. & Hebert, P. D. A DNA-based registry for all animal species: The barcode index number (BIN) system. PLoS ONE 8, e66213. https://doi.org/10.1371/journal.pone.0066213 (2013).ADS 
CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
74.Puillandre, N., Lambert, A., Brouillet, S. & Achaz, G. ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Mol. Ecol. 21, 1864–1877. https://doi.org/10.1111/j.1365-294X.2011.05239.x (2012).CAS 
Article 
PubMed 

Google Scholar 
75.Bouckaert, R. et al. BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. Plos Comput. Biol. 15, e1006650. https://doi.org/10.1371/journal.pcbi.1006650 (2019).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
76.Bouckaert, R. R. & Drummond, A. J. bModelTest: Bayesian phylogenetic site model averaging and model comparison. BMC Evol. Biol. 17, 42. https://doi.org/10.1186/s12862-017-0890-6 (2017).Article 
PubMed 
PubMed Central 

Google Scholar 
77.Rambaut, A., Drummond, A. J., Xie, D., Baele, G. & Suchard, M. A. Posterior summarization in bayesian phylogenetics using tracer 1.7. Syst. Biol. 67, 901–904. https://doi.org/10.1093/sysbio/syy032 (2018).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
78.Pons, J. et al. Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst. Biol. 55, 595–609. https://doi.org/10.1080/10635150600852011 (2006).Article 
PubMed 

Google Scholar 
79.Ezard, T., Fujisawa, T. & Barraclough, T. G. SPLITS: SPecies’ LImits by Threshold Statistics. R package version 1.0–18/r45 Available from: http://R-Forge.R-project.org/projects/splits/ (2009).80.Team, R. C. R: A language and environment for statistical computing, https://www.R-project.org/ (2020).81.Zhang, J., Kapli, P., Pavlidis, P. & Stamatakis, A. A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29, 2869–2876. https://doi.org/10.1093/bioinformatics/btt499 (2013).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
82.Kapli, P. et al. Multi-rate Poisson tree processes for single-locus species delimitation under maximum likelihood and Markov chain Monte Carlo. Bioinformatics 33, 1630–1638. https://doi.org/10.1093/bioinformatics/btx025 (2017).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
83.Jones, G. Algorithmic improvements to species delimitation and phylogeny estimation under the multispecies coalescent. J. Math. Biol. 74, 447–467. https://doi.org/10.1007/s00285-016-1034-0 (2017).MathSciNet 
Article 
PubMed 
MATH 

Google Scholar 
84.Jones, G., Aydin, Z. & Oxelman, B. DISSECT: An assignment-free Bayesian discovery method for species delimitation under the multispecies coalescent. Bioinformatics 31, 991–998. https://doi.org/10.1093/bioinformatics/btu770 (2015).CAS 
Article 
PubMed 

Google Scholar 
85.Rabosky, D. L. Automatic detection of key innovations, rate shifts, and diversity-dependence on phylogenetic trees. PLoS ONE 9, e89543. https://doi.org/10.1371/journal.pone.0089543 (2014).ADS 
CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
86.Rabosky, D. L. et al. BAMMtools: An R package for the analysis of evolutionary dynamics on phylogenetic trees. Methods Ecol. Evol. 5, 701–707. https://doi.org/10.1111/2041-210X.12199 (2014).Article 

Google Scholar 
87.Rozas, J. et al. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol. Biol. Evol. 34, 3299–3302. https://doi.org/10.1093/molbev/msx248 (2017).CAS 
Article 
PubMed 

Google Scholar 
88.Heled, J. & Drummond, A. Bayesian inference of population size history from multiple loci. BMC Evol. Biol. 8, 289 (2008).Article 

Google Scholar 
89.Leigh, J. W. & Bryant, D. POPART: Full-feature software for haplotype network construction. Methods Ecol. Evol. 6, 1110–1116. https://doi.org/10.1111/2041-210X.12410 (2015).Article 

Google Scholar 
90.Flot, J. F., Couloux, A. & Tillier, S. Haplowebs as a graphical tool for delimiting species: A revival of Doyle’s “field for recombination” approach and its application to the coral genus Pocillopora in Clipperton. BMC Evol. Biol. 10, 1. https://doi.org/10.1186/1471-2148-10-372 (2010).Article 

Google Scholar 
91.Stephens, M., Smith, N. J. & Donnelly, P. A new statistical method for haplotype reconstruction from population data. Am. J. Hum. Genet. 68, 978–989. https://doi.org/10.1086/319501 (2001).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
92.Spöri, Y. & Flot, J.-F. HaplowebMaker and CoMa: Two web tools to delimit species using haplowebs and conspecificity matrices. Methods Ecol. Evol. 11, 1434–1438. https://doi.org/10.1111/2041-210X.13454 (2020).Article 

Google Scholar  More

1.Lal, R. Soil carbon sequestration impacts on global climate change and food security. Science (80-). 304, 1623–1627 (2004).ADS 
CAS 
Article 

Google Scholar 
2.Janzen, H. H. Carbon cycling in earth systems—A soil science perspective. Agric. Ecosyst. Environ. 104, 399–417 (2004).CAS 
Article 

Google Scholar 
3.Leinweber, P., Jandl, G., Baum, C., Eckhardt, K. U. & Kandeler, E. Stability and composition of soil organic matter control respiration and soil enzyme activities. Soil Biol. Biochem. 40, 1496–1505 (2008).CAS 
Article 

Google Scholar 
4.Kosugi, Y. et al. Spatial and temporal variation in soil respiration in a Southeast Asian tropical rainforest. Agric. For. Meteorol. 147, 35–47 (2007).ADS 
Article 

Google Scholar 
5.Epron, D. Separating autotrophic and heterotrophic components of soil respiration: Lessons learned from trenching and related root-exclusion experiments. Soil Carbon Dyn. Integr. Methodol. https://doi.org/10.1017/CBO9780511711794.009 (2010).Article 

Google Scholar 
6.Musselman, R. C. & Fox, D. G. A review of the role of temperate forests in the global CO2 balance. J. Air Waste Manag. Assoc. 41, 798–807 (1991).CAS 
Article 

Google Scholar 
7.Lal, R. Carbon sequestration. Philos. Trans. R. Soc. B Biol. Sci. 363, 815–830 (2008).CAS 
Article 

Google Scholar 
8.Lal, R. Forest soils and carbon sequestration. For. Ecol. Manag. 220, 242–258 (2005).Article 

Google Scholar 
9.Kaiser, K., Guggenberger, G. & Zech, W. Sorption of DOM and DOM fractions to forest soils. Geoderma 74, 281–303 (1996).ADS 
Article 

Google Scholar 
10.Hassink, J. A model of the physical protection of organic matter in soils the capacity of soils to preserve organic C and N by their association with clay and silt particles. Plant Soil 191, 77–87 (1997).CAS 
Article 

Google Scholar 
11.Saidy, A. R. et al. Effects of clay mineralogy and hydrous iron oxides on labile organic carbon stabilisation. Geoderma 173–174, 104–110 (2012).ADS 
Article 
CAS 

Google Scholar 
12.Mueller, K. E. et al. Tree species effects on coupled cycles of carbon, nitrogen, and acidity in mineral soils at a common garden experiment. Biogeochemistry 111, 601–614 (2012).CAS 
Article 

Google Scholar 
13.Mulder, J., De Wit, H. A., Boonen, H. W. J. & Bakken, L. R. Increased levels of aluminium in forest soils: Effects on the stores of soil organic carbon. Water Air. Soil Pollut. 130, 989–994 (2001).ADS 
Article 

Google Scholar 
14.Gruba, P. & Socha, J. Exploring the effects of dominant forest tree species, soil texture, altitude, and pHH2O on soil carbon stocks using generalized additive models. For. Ecol. Manag. 447, 105–114 (2019).Article 

Google Scholar 
15.Chrzan, A. Zawartość wybranych metali ciężkich w glebie i faunie glebowej. Proc. ECOpole. 7, 23–26 (2013).
Google Scholar 
16.Ampoorter, E., Van Nevel, L., De Vos, B., Hermy, M. & Verheyen, K. Assessing the effects of initial soil characteristics, machine mass and traffic intensity on forest soil compaction. For. Ecol. Manag. 260, 1664–1676 (2010).Article 

Google Scholar 
17.Meriano, M., Eyles, N. & Howard, K. W. F. Hydrogeological impacts of road salt from Canada’s busiest highway on a Lake Ontario watershed (Frenchman’s Bay) and lagoon, City of Pickering. J. Contam. Hydrol. 107, 66–81 (2009).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
18.Barbier, L., Suaire, R., Durickovic, I., Laurent, J. & Simonnot, M. O. Is a road stormwater retention pond able to intercept deicing salt?. Water Air. Soil Pollut. 229, 1–12 (2018).CAS 
Article 

Google Scholar 
19.Willmert, H. M., Osso, J. D., Twiss, M. R. & Langen, T. A. Winter road management effects on roadside soil and vegetation along a mountain pass in the Adirondack Park, New York, USA. J. Environ. Manag. 225, 215–223 (2018).CAS 
Article 

Google Scholar 
20.General Directorate for National Roads and Motorways. Detailed technical specifications. Winter maintenance of the road network administered by the General Directorate for National Roads and Motorways, Lublin Branch in the years: 2012÷2016 (in Polish). (2012).21.Durickovic, I. NaCl material for winter maintenance and its environmental effect. Salt Earth https://doi.org/10.5772/intechopen.86907 (2020).Article 

Google Scholar 
22.General Directorate for National Roads and Motorways. We’ll recap the winter of 2019/2020 and explain what road maintenance is all about (in Polish). (2020). https://www.archiwum.gddkia.gov.pl/pl/a/37500/Podsumujemy-zime-20192020-i-wyjasnimy-o-co-chodzi-w-utrzymaniu-drog. Accessed on October 20, 2021.23.General Directorate for National Roads and Motorways. Ready for all weather. The 2020/2021 winter season has begun (in Polish). (2020). https://www.archiwum.gddkia.gov.pl/pl/a/40259/Gotowi-na-kazda-pogode-Zaczal-sie-sezon-zimowy-20202021. Accessed on October 20, 2021.24.General Directorate for National Roads and Motorways. Average annual daily traffic (AADT) at measuring points in 2015 on state roads (in Polish). (2015). https://www.archiwum.gddkia.gov.pl/pl/2551/GPR-2015. Accessed on October 20, 2021.25.QGIS Association. QGIS Geographic Information System. (2021). http://www.qgis.org Accessed on October 20, 2021.26.Woś, A. The Climate of Poland (in Polish) (Polish Scientific Publishers PWN, 1999).
Google Scholar 
27.Polish State Forests. Nature and forest conditions of Suchedniów Forest Inspectorate (in Polish). A report. (2011). https://suchedniow.radom.lasy.gov.pl/documents/11058/18775352/warunki+przyrodniczo-lesne.pdf Accessed on October 20, 2021.28.Hopkins, D. W. Carbon mineralization. In Soil Sampling and Methods of Analysis (eds. Carter, M. R. & Gregorich, E. G.) (CRC Press, 2008).29.Buurman, P., van Lagen, B. & Velthorst, E. J. Manual for Soil and Water Analysis (Backhuys Publishers, 1996).
Google Scholar 
30.R Core Team (2021). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ Accessed on October 20, 2021..31.Navrátil, T. et al. Soil mercury distribution in adjacent coniferous and deciduous stands highly impacted by acid rain in the Ore Mountains, Czech Republic. Appl. Geochem. 75, 63–75 (2016).Article 
CAS 

Google Scholar 
32.Gruba, P., Pietrzykowski, M. & Pasichnyk, D. Tree species affects the concentration of total mercury (Hg) in forest soils: Evidence from a forest soil inventory in Poland. Sci. Total Environ. 647, 141–148 (2019).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
33.Obrist, D. et al. Mercury distribution across 14 U.S. Forests. Part I: Spatial patterns of concentrations in biomass, litter, and soils. Environ. Sci. Technol. 45, 3974–3981 (2011).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
34.Kupka, D., Kania, M., Pietrzykowski, M., Łukasik, A. & Gruba, P. Multiple factors influence the accumulation of heavy metals (Cu, Pb, Ni, Zn) in forest soils in the vicinity of roadways. Water Air Soil Pollut. 232, 1–13 (2021).Article 
CAS 

Google Scholar 
35.Borchers, J. G. & Perry, A. D. The influence of soil texture and aggregation on carbon and nitrogen dynamics in southwest Oregon forests and clearcuts. Can. J. For. Res. 22, 298–305 (1992).CAS 
Article 

Google Scholar 
36.Chantigny, M. H., Angers, D. A., Kaiser, K. & Kalbitz, K. Extraction and characterization of dissolved organic matter. In Soil Sampling and Methods of Analysis (eds. Carter, M. & Gregorich, E. G.) (CRC Press, 2008).37.Zehetner, F., Rosenfellner, U., Mentler, A. & Gerzabek, M. H. Distribution of road salt residues, heavy metals and polycyclic aromatic hydrocarbons across a highway-forest interface. Water Air Soil Pollut. 198, 125–132 (2009).ADS 
CAS 
Article 

Google Scholar 
38.Grigalaviciene, I., Rutkoviene, V. & Marozas, V. The accumulation of heavy metals Pb, Cu and Cd at roadside forest soil. Polish J. Environ. Stud. 14, 109–115 (2005).CAS 

Google Scholar 
39.Bäckström, M., Bäckman, L., Folkeson, L., Karlsson, S. & Lind, B. Mobilisation of heavy metals by deicing salts in a roadside environment. Water Res. 38, 720–732 (2004).PubMed 
Article 
CAS 

Google Scholar 
40.Singh, D. V., Bhat, J. I. A., Bhat, R. A., Dervash, M. A. & Ganei, S. A. Vehicular stress a cause for heavy metal accumulation and change in physico-chemical characteristics of road side soils in Pahalgam. Environ. Monit. Assess. 190, 1–10 (2018).Article 
CAS 

Google Scholar 
41.Doelman, P. & Haanstra, L. Short-term and long-term effects of cadmium, chromium, copper, nickel, lead and zinc on soil microbial respiration in relation to abiotic soil factors. Plant Soil 79, 317–327 (1984).CAS 
Article 

Google Scholar 
42.Hattori, H. Influence of heavy metals on soil mcrobial activities. Soil Sci. Plant Nutr. 38, 93–100 (1992).CAS 
Article 

Google Scholar 
43.Gülser, F. & Erdoǧan, E. The effects of heavy metal pollution on enzyme activities and basal soil respiration of roadside soils. Environ. Monit. Assess. 145, 127–133 (2008).PubMed 
Article 
CAS 
PubMed Central 

Google Scholar 
44.Lofgren, S. The chemical effects of deicing salt on soil and stream water of five catchments in southeast Sweden. Water Air Soil Pollut. 130, 863–868 (2001).ADS 
Article 

Google Scholar 
45.Mason, C. F., Norton, S. A., Fernandez, I. J. & Katz, L. E. Deconstruction of the chemical effects of road salt on stream water chemistry. J. Environ. Qual. 28, 82–91 (1999).CAS 
Article 

Google Scholar 
46.Robinson, H. K., Hasenmueller, E. A. & Chambers, L. G. Soil as a reservoir for road salt retention leading to its gradual release to groundwater. Appl. Geochem. 83, 72–85 (2017).CAS 
Article 

Google Scholar 
47.Rhodes, A. L. & Guswa, A. J. Storage and release of road-salt contamination from a calcareous lake-basin fen, western Massachusetts, USA. Sci. Total Environ. 545–546, 525–545 (2016).ADS 
PubMed 
Article 
CAS 
PubMed Central 

Google Scholar 
48.Cunningham, M. A., Snyder, E., Yonkin, D., Ross, M. & Elsen, T. Accumulation of deicing salts in soils in an urban environment. Urban Ecosyst. 11, 17–31 (2008).Article 

Google Scholar 
49.Berggren, D., Mulder, J. & Westerhof, R. Prolonged leaching of mineral forest soils with dilute HCl solutions: The solubility of Al and soil organic matter. Eur. J. Soil Sci. 49, 305–316 (1998).CAS 
Article 

Google Scholar 
50.Prenzel, J. & Schulte-Bisping, H. Some chemical parameter relations in a population of German forest soils. Geoderma 64, 309–326 (1995).ADS 
CAS 
Article 

Google Scholar 
51.Reuss, J. O., Walthall, P. M., Roswall, E. C. & Hopper, R. W. E. Aluminum solubility, calcium-aluminum exchange, and pH in acid forest soils. Soil Sci. Soc. Am. J. 54, 374–380 (1990).ADS 
CAS 
Article 

Google Scholar 
52.Hobbie, S. E. et al. Tree species effects on soil organic matter dynamics: The role of soil cation composition. Ecosystems 10, 999–1018 (2007).CAS 
Article 

Google Scholar 
53.Scheel, T., Jansen, B., Van Wijk, A. J., Verstraten, J. M. & Kalbitz, K. Stabilization of dissolved organic matter by aluminium: A toxic effect or stabilization through precipitation?. Eur. J. Soil Sci. 59, 1122–1132 (2008).CAS 
Article 

Google Scholar 
54.Lützow, M. V. et al. Stabilization of organic matter in temperate soils: Mechanisms and their relevance under different soil conditions—A review. Eur. J. Soil Sci. 57, 426–445 (2006).Article 
CAS 

Google Scholar 
55.Gruba, P. & Socha, J. Effect of parent material on soil acidity and carbon content in soils under silver fir (Abies alba Mill.) stands in Poland. CATENA 140, 90–95 (2016).CAS 
Article 

Google Scholar 
56.Gruba, P. & Mulder, J. Tree species affect cation exchange capacity (CEC) and cation binding properties of organic matter in acid forest soils. Sci. Total Environ. 511, 655–662 (2015).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
57.Reich, P. B. et al. Linking litter calcium, earthworms and soil properties: A common garden test with 14 tree species. Ecol. Lett. 8, 811–818 (2005).Article 

Google Scholar  More

1.Jarvis, E. D. et al. Whole-genome analyses resolve early branches in the tree of life of modern birds. Science 346, 1320–1331 (2014).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
2.Jetz, W., Thomas, G. H., Joy, J. B., Hartmann, K. & Mooers, A. O. The global diversity of birds in space and time. Nature 491, 444–448 (2012).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
3.Claramunt, S. & Cracraft, J. A new time tree reveals Earth history’s imprint on the evolution of modern birds. Sci. Adv. 1, e1501005 (2015).ADS 
PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
4.Jenni, L. & Winkler, R. Moult and Ageing of European Passerines. (Bloomsbury Publishing, 2020).5.Ginn, H. B. & Melville, D. S. Moult in Birds (BTO guide). (British Trust for Ornithology, 1983).6.Stresemann, E. & Stresemann, V. Die Mauser der Vögel. (Friedländer, 1966).7.Jenni, L. & Winkler, R. The Biology of Moult in Birds. (Bloomsbury Publishing, 2020).8.Kiat, Y., Izhaki, I. & Sapir, N. The effects of long-distance migration on the evolution of moult strategies in Western-Palearctic passerines. Biol. Rev. 94, 700–720 (2019).PubMed 
Article 
PubMed Central 

Google Scholar 
9.Kiat, Y. et al. Sequential molt in a feathered dinosaur and implications for early paravian ecology and locomotion. Curr. Biol. 30, 3633–3638 (2020).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
10.Pyle, P. Identification guide to North American birds: A Compendium of Information on Identifying, Ageing, and Sexing ‘Near-Passerines’ and Passerines in the Hand. (Slate Creek Press, 1997).11.Berlow, E. L., Brose, U. & Martinez, N. D. The, “Goldilocks factor” in food webs. Proc. Natl. Acad. Sci. 105, 4079–4080 (2008).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
12.Dale, J., Dey, C. J., Delhey, K., Kempenaers, B. & Valcu, M. The effects of life history and sexual selection on male and female plumage colouration. Nature 529, 367–370 (2015).ADS 
Article 
CAS 

Google Scholar 
13.Kleiber, M. Body size and metabolism. Hilgardia 6, 315–353 (1932).CAS 
Article 

Google Scholar 
14.McKinnon, L. et al. Lower predation risk for migratory birds at high latitudes. Science 327, 326–327 (2010).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
15.Meiri, S., Dayan, T. & Simberloff, D. Biogeographical patterns in the Western Palearctic: the fasting-endurance hypothesis and the status of Murphy’s rule. J. Biogeogr. 32, 369–375 (2005).Article 

Google Scholar 
16.Millar, J. S. & Hickling, G. J. Fasting endurance and the evolution of mammalian body size. Funct. Ecol. 4, 5–12 (1990).Article 

Google Scholar 
17.Peters, R. H. & Peters, R. H. The Ecological Implications of Body Size. vol. 2 (Cambridge University Press, 1986).18.Pérez-Granados, C. et al. Time available for moulting shapes inter- and intra-specific variability in post-juvenile moult extent in wheatears (genus Oenanthe). J. Ornithol. 162, 255–264 (2020).Article 

Google Scholar 
19.Hemborg, C., Sanz, J. & Lundberg, A. Effects of latitude on the trade-off between reproduction and moult: a long-term study with Pied Flycatcher. Oecologia 129, 206–212 (2001).ADS 
PubMed 
Article 
PubMed Central 

Google Scholar 
20.de la Hera, I., Díaz, J. a., Pérez-Tris, J. & Tellería, J. L. A comparative study of migratory behaviour and body mass as determinants of moult duration in passerines. J. Avian Biol. 40, 461–465 (2009).21.Kiat, Y. & Sapir, N. Age-dependent modulation of songbird summer feather moult by temporal and functional constraints. Am. Nat. 189, 184–195 (2017).PubMed 
Article 
PubMed Central 

Google Scholar 
22.Møller, A. P. The allometry of number of feathers in birds changes seasonally. Avian Res. 6, 1–5 (2015).Article 

Google Scholar 
23.Rohwer, S., Ricklefs, R. E., Rohwer, V. G. & Copple, M. M. Allometry of the duration of flight feather molt in birds. PLoS Biol. 7, 1246 (2009).Article 
CAS 

Google Scholar 
24.Rohwer, V. G. & Rohwer, S. How do birds adjust the time required to replace their flight feathers?. Auk 130, 699–707 (2013).Article 

Google Scholar 
25.Barta, Z. et al. Annual routines of non-migratory birds: optimal moult strategies. Oikos 112, 580–593 (2006).Article 

Google Scholar 
26.Barta, Z. et al. Optimal moult strategies in migratory birds. Philos. Trans. R. Soc. London B Biol. Sci. 363, 211–229 (2008).27.Wunderle, J. M. Age-specific foraging proficiency in birds. Curr. Ornithol. 8, 273–324 (1991).
Google Scholar 
28.Marchetti, K. & Price, T. Differences in the foraging of juvenile and adult birds: the importance of developmental constraints. Biol. Rev. 64, 51–70 (1989).Article 

Google Scholar 
29.Delhey, K. et al. Partial or complete? The evolution of post-juvenile moult strategies in passerine birds. J. Anim. Ecol. 89, 2896–2908 (2020).PubMed 
Article 
PubMed Central 

Google Scholar 
30.Kiat, Y. & Izhaki, I. Why renew fresh feathers? Advantages and conditions for the evolution of complete post-juvenile moult. J. Avian Biol. 47, 47–56 (2016).Article 

Google Scholar 
31.Kiat, Y. & Sapir, N. Life-history trade-offs result in evolutionary optimization of feather quality. Biol. J. Linn. Soc. 125, 613–624 (2018).
Google Scholar 
32.Callan, L. M., La Sorte, F. A., Martin, T. E. & Rohwer, V. G. Higher nest predation favors rapid fledging at the cost of plumage quality in nestling birds. Am. Nat. 193, 717–724 (2019).PubMed 
Article 
PubMed Central 

Google Scholar 
33.Del Hoyo, J., Elliott, A., Sargatal, J., Christie, D. A. & de Juana, E. Handbook of the Birds of the World Alive (Lynx Edicions, 2019).
Google Scholar 
34.Dunning Jr, J. B. CRC Handbook of Avian Body Masses. (CRC Press, 2007).35.Billerman, S. M., Keeney, B. K., Rodewald, P. G. & Schulenberg, T. S. Birds of the World. (Cornell Laboratory of Ornithology, 2020).36.Bird species distribution maps of the world. BirdLife International (2019).37.Jetz, W. et al. Global distribution and conservation of evolutionary distinctness in birds. Curr. Biol. 24, 919–930 (2014).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
38.Rubolini, D., Liker, A., Garamszegi, L. Z., Møller, A. P. & Saino, N. Using the BirdTree.org website to obtain robust phylogenies for avian comparative studies: a primer. Curr. Zool. 61, 959–965 (2015).39.Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).Article 

Google Scholar 
40.Akaike, H. Factor analysis and AIC. Psychometrika 52, 317–332 (1987).MathSciNet 
MATH 
Article 

Google Scholar 
41.Rabosky, D. L. No substitute for real data: a cautionary note on the use of phylogenies from birth–death polytomy resolvers for downstream comparative analyses. Evolution 69, 3207–3216 (2015).PubMed 
Article 
PubMed Central 

Google Scholar 
42.Thomas, G. H. An avian explosion. Nature 526, 516–517 (2015).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
43.Prum, R. O. et al. A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature 526, 569–573 (2015).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
44.Ives, A. R. & Garland, T. Jr. Phylogenetic logistic regression for binary dependent variables. Syst. Biol. 59, 9–26 (2010).PubMed 
Article 
PubMed Central 

Google Scholar 
45.Tung Ho, L. si & Ané, C. A linear-time algorithm for Gaussian and non-Gaussian trait evolution models. Syst. Biol. 63, 397–408 (2014).46.Felsenstein, J. A comparative method for both discrete and continuous characters using the threshold model. Am. Nat. 179, 145–156 (2012).PubMed 
Article 
PubMed Central 

Google Scholar 
47.Cody, M. L. A general theory of clutch size. Evolution 174–184 (1966).48.Newton, I. The Migration Ecology of Birds. (Academic Press, 2010).49.Newton, I. Speciation and Biogeography of Birds. (Academic Press, 2003).50.Terrill, R. S., Seeholzer, G. F. & Wolfe, J. D. Evolution of breeding plumages in birds: a multiple-step pathway to seasonal dichromatism in New World warblers (Aves: Parulidae). Ecol. Evol. 10, 9223–9239 (2020).PubMed 
PubMed Central 
Article 

Google Scholar 
51.Fogden, M. P. L. The seasonality and population dynamics of equatorial forest birds in Sarawak. Ibis 114, 307–343 (1972).Article 

Google Scholar 
52.Kiat, Y., Davaasuren, B., Erdenechimeg, T., Troupin, D. & Sapir, N. Large-scale longitudinal climate gradient across the Palearctic region affects passerine feather moult extent. Ecography 44, 124–133 (2020).Article 

Google Scholar 
53.Kiat, Y., Vortman, Y. & Sapir, N. Feather moult and bird appearance are correlated with global warming over the last 200 years. Nat. Commun. 10, 1–7 (2019).ADS 
CAS 
Article 

Google Scholar 
54.Bojarinova, J. G., Lehikoinen, E. & Eeva, T. Dependence of postjuvenile moult on hatching date, condition and sex in the Great Tit. J. Avian Biol. 30, 437–446 (1999).Article 

Google Scholar 
55.Ryzhanovsky, V. N. Subspecies-specific features of molt in the Common Chiffchaff (Phylloscopus collybita) from Europe and Western Siberia. Russ. J. Ecol. 48, 268–274 (2017).Article 

Google Scholar 
56.Slavenko, A. et al. Global patterns of body size evolution in squamate reptiles are not driven by climate. Glob. Ecol. Biogeogr. 28, 471–483 (2019).Article 

Google Scholar 
57.Graham, C. H., Storch, D. & Machac, A. Phylogenetic scale in ecology and evolution. Glob. Ecol. Biogeogr. 27, 175–187 (2018).Article 

Google Scholar 
58.Hone, D. W. E., Dyke, G. J., Haden, M. & Benton, M. J. Body size evolution in Mesozoic birds. J. Evol. Biol. 21, 618–624 (2008).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
59.Xu, X. et al. An integrative approach to understanding bird origins. Science 346, 1253293 (2014).PubMed 
Article 
CAS 
PubMed Central 

Google Scholar 
60.Berv, J. S. & Field, D. J. Genomic signature of an avian Lilliput effect across the K-Pg extinction. Syst. Biol. 67, 1–13 (2018).PubMed 
Article 
PubMed Central 

Google Scholar 
61.Dececchi, T. A. & Larsson, H. C. E. Body and limb size dissociation at the origin of birds: uncoupling allometric constraints across a macroevolutionary transition. Evolution 67, 2741–2752 (2013).PubMed 
Article 
PubMed Central 

Google Scholar 
62.Puttick, M. N., Thomas, G. H. & Benton, M. J. High rates of evolution preceded the origin of birds. Evolution 68, 1497–1510 (2014).PubMed 
PubMed Central 
Article 

Google Scholar 
63.Vizcaíno, S. F. & Fariña, R. A. On the flight capabilities and distribution of the giant Miocene bird Argentavis magnificens (Teratornithidae). Lethaia 32, 271–278 (1999).Article 

Google Scholar 
64.McNeill Alexander, R. All-time giants: the largest animals and their problems. Palaeontology 41, 1231–1246 (1998).
Google Scholar  More

1.Serreze, M. C. & Meier, W. N. The Arctic’s sea ice cover: trends, variability, predictability, and comparisons to the Antarctic. Ann. N. Y. Acad. Sci. 1436, 36–53 (2019).PubMed 
Article 
PubMed Central 

Google Scholar 
2.Pörtner, H. et al. IPCC, 2019: IPCC Special Report on the Ocean and Cryosphere in a Changing Climate. Intergov. Panel Clim. Chang. 1–765 (2019).3.Kwok, R. Arctic sea ice thickness, volume, and multiyear ice coverage: losses and coupled variability (1958–2018). Environ. Res. Lett. 13, 105005 (2018).Article 

Google Scholar 
4.Wassmann, P. & Reigstad, M. Future Arctic Ocean seasonal ice zones and implications for pelagic-benthic coupling. Oceanography 24, 220–231 (2011).Article 

Google Scholar 
5.Nöthig, E.-M. et al. Summertime plankton ecology in Fram Strait—a compilation of long- and short-term observations. Polar Res. 34, 23349 (2015).Article 
CAS 

Google Scholar 
6.Assmy, P. et al. Leads in Arctic pack ice enable early phytoplankton blooms below snow-covered sea ice. Sci. Rep. 7, 40850 (2017).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
7.Neukermans, G., Oziel, L. & Babin, M. Increased intrusion of warming Atlantic water leads to rapid expansion of temperate phytoplankton in the Arctic. Glob. Chang. Biol. 24, 2545–2553 (2018).PubMed 
Article 

Google Scholar 
8.Wiedmann, I. et al. What feeds the Benthos in the Arctic Basins? Assembling a carbon budget for the deep Arctic Ocean. Front. Mar. Sci. 7, 544386 (2020).9.Randelhoff, A. & Sundfjord, A. Short commentary on marine productivity at Arctic shelf breaks: upwelling, advection and vertical mixing. Ocean Sci. 14, 293–300 (2018).Article 

Google Scholar 
10.Lewis, K. M., van Dijken, G. L. & Arrigo, K. R. Changes in phytoplankton concentration now drive increased Arctic Ocean primary production. Sci. (80-.). 369, 198–202 (2020).Article 
CAS 

Google Scholar 
11.Arrigo, K. R. & van Dijken, G. L. Continued increases in Arctic Ocean primary production. Prog. Oceanogr. 136, 60–70 (2015).Article 

Google Scholar 
12.Leu, E. et al. Arctic spring awakening—steering principles behind the phenology of vernal ice algal blooms. Prog. Oceanogr. 139, 151–170 (2015).Article 

Google Scholar 
13.Arrigo, K. R. et al. Massive phytoplankton blooms under Arctic sea ice. Science 336, 1408–1408 (2012).PubMed 
Article 
CAS 
PubMed Central 

Google Scholar 
14.Lalande, C. et al. Variability in under-ice export fluxes of biogenic matter in the Arctic Ocean. Glob. Biogeochem. Cycles 28, 571–583 (2014).Article 
CAS 

Google Scholar 
15.Fernández-Méndez, M. et al. Photosynthetic production in the central Arctic Ocean during the record sea-ice minimum in 2012. Biogeosciences 12, 3525–3549 (2015).Article 

Google Scholar 
16.Boetius, A. et al. Export of algal biomass from the melting Arctic sea ice. Science 339, 1430–1432 (2013).PubMed 
Article 
CAS 
PubMed Central 

Google Scholar 
17.Assmy, P. et al. Floating ice-algal aggregates below melting Arctic sea ice. PLoS ONE 8, e76599 (2013).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
18.Perrette, M., Yool, A., Quartly, G. D. & Popova, E. E. Near-ubiquity of ice-edge blooms in the Arctic. Biogeosciences 8, 515–524 (2011).Article 

Google Scholar 
19.Underwood, G. J. C. et al. Organic matter from Arctic sea-ice loss alters bacterial community structure and function. Nat. Clim. Chang. 9, 170–176 (2019).Article 

Google Scholar 
20.Herndl, G. J. & Reinthaler, T. Microbial control of the dark end of the biological pump. Nat. Geosci. 6, 718–724 (2013).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
21.Henson, S., Le Moigne, F. & Giering, S. Drivers of carbon export efficiency in the global ocean. Glob. Biogeochem. Cycles 33, 891–903 (2019).Article 
CAS 

Google Scholar 
22.Ruiz‐González, C. et al. Major imprint of surface plankton on deep ocean prokaryotic structure and activity. Mol. Ecol. 29, 1820–1838 (2020).PubMed 
Article 
CAS 

Google Scholar 
23.Mestre, M. et al. Sinking particles promote vertical connectivity in the ocean microbiome. Proc. Natl Acad. Sci. USA 115, E6799–E6807 (2018).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
24.Preston, C. M., Durkin, C. A. & Yamahara, K. M. DNA metabarcoding reveals organisms contributing to particulate matter flux to abyssal depths in the North East Pacific ocean. Deep Sea Res. Part II Top. Stud. Oceanogr. 173, 104708 (2020).Article 
CAS 

Google Scholar 
25.Poff, K. E., Leu, A. O., Eppley, J. M., Karl, D. M. & DeLong, E. F. Microbial dynamics of elevated carbon flux in the open ocean’s abyss. Proc. Natl Acad. Sci. USA 118, 1–11 (2021).Article 
CAS 

Google Scholar 
26.Boeuf, D. et al. Biological composition and microbial dynamics of sinking particulate organic matter at abyssal depths in the oligotrophic open ocean. Proc. Natl Acad. Sci. USA 116, 11824–11832 (2019).PubMed 
PubMed Central 
CAS 

Google Scholar 
27.Thiele, S., Fuchs, B. M., Amann, R. & Iversen, M. H. Colonization in the photic zone and subsequent changes during sinking determine bacterial community composition in marine snow. Appl. Environ. Microbiol. 81, 1463–1471 (2015).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
28.Rapp, J. Z., Fernández-Méndez, M., Bienhold, C. & Boetius, A. Effects of ice-algal aggregate export on the connectivity of bacterial communities in the central Arctic Ocean. Front. Microbiol. 9, 1035 (2018).29.Smedsrud, L. H., Halvorsen, M. H., Stroeve, J. C., Zhang, R. & Kloster, K. Fram Strait sea ice export variability and September Arctic sea ice extent over the last 80 years. Cryosphere 11, 65–79 (2017).Article 

Google Scholar 
30.Krumpen, T. et al. Arctic warming interrupts the Transpolar Drift and affects long-range transport of sea ice and ice-rafted matter. Sci. Rep. 9, 5459 (2019).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
31.Lalande, C. et al. Lateral supply and downward export of particulate matter from upper waters to the seafloor in the deep eastern Fram Strait. Deep Sea Res. Part I Oceanogr. Res. Pap. 114, 78–89 (2016).Article 

Google Scholar 
32.Wekerle, C., Krumpen, T., Dinter, T., Iversen, M. & Salter, I. Origin and properties of sediment trap catchment areas in Fram Strait: results from Lagrangian modelling and remote sensing. Front. Mar. Sci. 5, 4071– 26 (2018).33.Callahan, B. J. et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
34.Hsieh, T. C., Ma, K. H. & Chao, A. iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods Ecol Evol, 7, 1451–1456 (2016).Article 

Google Scholar 
35.Wilson, B. et al. Changes in marine prokaryote composition with season and depth over an Arctic polar year. Front. Mar. Sci. 4, 1–17 (2017).
Google Scholar 
36.Leu, E., Søreide, J. E., Hessen, D. O., Falk-Petersen, S. & Berge, J. Consequences of changing sea-ice cover for primary and secondary producers in the European Arctic shelf seas: Timing, quantity, and quality. Prog. Oceanogr. 90, 18–32 (2011).Article 

Google Scholar 
37.Becagli, S. et al. Relationships linking primary production, sea ice melting, and biogenic aerosol in the Arctic. Atmos. Environ. 136, 1–15 (2016).Article 
CAS 

Google Scholar 
38.Lalande, C., Bauerfeind, E., Nöthig, E. & Beszczynska-Möller, A. Impact of a warm anomaly on export fluxes of biogenic matter in the eastern Fram Strait. Prog. Oceanogr. 109, 70–77 (2013).Article 

Google Scholar 
39.Olli, K. et al. Food web functions and interactions during spring and summer in the Arctic water inflow region: investigated through inverse modeling. Front. Mar. Sci. 6, https://doi.org/10.3389/fmars.2019.00244 (2019).40.Bauerfeind, E. et al. Particle sedimentation patterns in the eastern Fram Strait during 2000 – 2005: Results from the Arctic long-term observatory HAUSGARTEN. Deep Sea Res. Part I 56, 1471–1487 (2009).Article 
CAS 

Google Scholar 
41.Soltwedel, T. et al. Natural variability or anthropogenically-induced variation? Insights from 15 years of multidisciplinary observations at the arctic marine LTER site HAUSGARTEN. Ecol. Indic. 1–14, https://doi.org/10.1016/j.ecolind.2015.10.001 (2015).42.Randelhoff, A. et al. Arctic mid-winter phytoplankton growth revealed by autonomous profilers. Sci. Adv. 6, eabc2678 (2020).PubMed 
PubMed Central 
Article 

Google Scholar 
43.Tedesco, L., Vichi, M. & Scoccimarro, E. Sea-ice algal phenology in a warmer Arctic. Sci. Adv. 5, eaav4830 (2019).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
44.Lannuzel, D. et al. The future of Arctic sea-ice biogeochemistry and ice-associated ecosystems. Nat. Clim. Chang. 10, 983–992 (2020).Article 

Google Scholar 
45.Martin, J. H., Knauer, G. A., Karl, D. M. & Broenkow, W. W. VERTEX: carbon cycling in the northeast Pacific. Deep Sea Res. A: Oceanogr. Res. Pap. 34, 267–285 (1987).Article 
CAS 

Google Scholar 
46.Polyakov, I. V. et al. Greater role for Atlantic inflows on sea-ice loss in the Eurasian Basin of the Arctic. Ocean. Science 356, 285–291 (2017).PubMed 
CAS 

Google Scholar 
47.Wang, Q. et al. The Finite Element Sea Ice-Ocean Model (FESOM) v.1.4: formulation of an ocean general circulation model. Geosci. Model Dev. 7, 663–693 (2014).Article 
CAS 

Google Scholar 
48.Wekerle, C. et al. Eddy-resolving simulation of the Atlantic water circulation in the Fram Strait with focus on the seasonal cycle. J. Geophys. Res. Ocean. 122, 8385–8405 (2017).Article 

Google Scholar 
49.Iversen, M. H. & Ploug, H. Temperature effects on carbon-specific respiration rate and sinking velocity of diatom aggregates – potential implications for deep ocean export processes. Biogeosciences 10, 4073–4085 (2013).Article 

Google Scholar 
50.Briggs, N., Dall’Olmo, G. & Claustre, H. Major role of particle fragmentation in regulating biological sequestration of CO 2 by the oceans. Science 367, 791–793 (2020).PubMed 
Article 
CAS 

Google Scholar 
51.Fadeev, E. et al. Microbial communities in the East and West Fram Strait during sea ice melting season. Front. Mar. Sci. 5, 429 (2018).52.Buchan, A., LeCleir, G. R., Gulvik, C. A., González, J. M. & Gonzalez, J. M. Master recyclers: features and functions of bacteria associated with phytoplankton blooms. Nat. Rev. Microbiol. 12, 686–698 (2014).PubMed 
Article 
CAS 

Google Scholar 
53.Bergauer, K. et al. Organic matter processing by microbial communities throughout the Atlantic water column as revealed by metaproteomics. Proc. Natl Acad. Sci. 115, E400–E408 (2018).PubMed 
Article 
CAS 

Google Scholar 
54.Zhao, Z., Baltar, F. & Herndl, G. J. Linking extracellular enzymes to phylogeny indicates a predominantly particle-associated lifestyle of deep-sea prokaryotes. Sci. Adv. 6, 1–11 (2020).CAS 

Google Scholar 
55.Hatzenpichler, R. Diversity, physiology, and niche differentiation of ammonia-oxidizing archaea. Appl. Environ. Microbiol. 78, 7501–7510 (2012).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
56.Brown, C. M., Mathai, P. P., Loesekann, T., Staley, C. & Sadowsky, M. J. Influence of library composition on sourcetracker predictions for community-based microbial source tracking. Environ. Sci. Technol. 53, 60–68 (2019).PubMed 
Article 
CAS 
PubMed Central 

Google Scholar 
57.Słomka, J., Alcolombri, U., Secchi, E., Stocker, R. & Fernandez, V. I. Encounter rates between bacteria and small sinking particles. N. J. Phys. 22, 043016 (2020).Article 

Google Scholar 
58.Datta, M. S., Sliwerska, E., Gore, J., Polz, M. F. & Cordero, O. X. Microbial interactions lead to rapid micro-scale succesions on model marine particles. Nat. Commun. 7, 1–7 (2016).Article 
CAS 

Google Scholar 
59.Ploug, H., Iversen, M. H. & Fischer, G. Ballast, sinking velocity, and apparent diffusivity within marine snow and zooplankton fecal pellets: Implications for substrate turnover by attached bacteria. Limnol. Oceanogr. 53, 1878–1886 (2008).Article 

Google Scholar 
60.Kiørboe, T., Tang, K., Grossart, H. & Ploug, H. Dynamics of microbial communities on marine snow aggregates: colonization, growth, detachment, and grazing mortality of attached bacteria. Appl. Environ. Microbiol. 69, 3036–3047 (2003).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
61.Proctor, L. M. & Fuhrman, J. A. Roles of viral infection in organic particle flux. Mar. Ecol. Prog. Ser. 69, 133–142 (1991).Article 

Google Scholar 
62.Tamburini, C. et al. Effects of hydrostatic pressure on microbial alteration of sinking fecal pellets. Deep Sea Res. Part II: Top. Stud. Oceanogr. 56, 1533–1546 (2009).Article 
CAS 

Google Scholar 
63.Grossart, H. P. & Gust, G. Hydrostatic pressure affects physiology and community structure of marine bacteria during settling to 4000 m: An experimental approach. Mar. Ecol. Prog. Ser. 390, 97–104 (2009).Article 

Google Scholar 
64.Bochdansky, A. B., Clouse, M. A. & Herndl, G. J. Dragon kings of the deep sea: marine particles deviate markedly from the common number-size spectrum. Sci. Rep. 6, 4–10 (2016).Article 
CAS 

Google Scholar 
65.Zinger, L., Boetius, A. & Ramette, A. Bacterial taxa-area and distance-decay relationships in marine environments. Mol. Ecol. 23, 954–964 (2014).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
66.Hoffmann, K. et al. Diversity and metabolism of Woeseiales bacteria, global members of marine sediment communities. ISME J. 14, 1042–1056 (2020).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
67.Spreen, G., Kaleschke, L. & Heygster, G. Sea ice remote sensing using AMSR-E 89-GHz channels. J. Geophys. Res. 113, C02S03 (2008).
Google Scholar 
68.Cavalieri, D. J., Parkinson, C. L., Gloersen, P. & Zwally, H. J. Sea Ice Concentrations from Nimbus-7 SMMR and DMSP SSM/I-SSMIS Passive Microwave Data, Version 1. (1996). https://doi.org/10.5067/8GQ8LZQVL0VL69.Edler, L. Recommendations on Methods for Marine Biological Studies in the Baltic Sea. Phytoplankton and Chlorophyll. (Baltic Marine Biologists BMB, Sweden) (1979).70.Ploug, H. & Jørgensen, B. B. A net-jet flow system for mass transfer and micro electrode studies in sinking aggregates. Mar. Ecol. Prog. Ser. 176, 279 (1999).Article 
CAS 

Google Scholar 
71.Parada, A. E., Needham, D. M. & Fuhrman, J. A. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ. Microbiol. 18, 1403–1414 (2016).PubMed 
Article 
CAS 
PubMed Central 

Google Scholar 
72.Fadeev, E. et al. Comparison of two 16S rRNA Primers (V3–V4 and V4–V5) for studies of Arctic microbial communities. Front. Microbiol. 12, 1–11 (2021).Article 

Google Scholar 
73.Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. J. 17, 10 (2011).Article 

Google Scholar 
74.Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, 590–596 (2013).75.McMurdie, P. J. & Holmes, S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8, e61217 (2013).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
76.Gómez-Rubio, V. ggplot2—elegant graphics for data analysis (2nd edition). J. Statistical Softw. 77, (2017).77.McMurdie, P. J. & Holmes, S. Waste not, want not: why rarefying microbiome data is inadmissible. PLoS Comput. Biol. 10, e1003531 (2014).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
78.Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).PubMed 
PubMed Central 

Google Scholar 
79.Knights, D. et al. Bayesian community-wide culture-independent microbial source tracking. Nat. Methods 8, 761–763 (2011).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
80.Silvester, N. et al. The European Nucleotide Archive in 2017. Nucleic Acids Res. 46, D36–D40 (2018).PubMed 
Article 
CAS 

Google Scholar 
81.Diepenbroek, M. et al. in Informatik 2014 (eds. Plödereder, E., Grunske, L., Schneider, E. & Ull, D.) 1711–1721 (Gesellschaft für Informatik e.V., 2014).82.Wekerle, C. Backward particle trajectories used to estimate the pathways of settling aggregates measured at stations N, HG and EG in Fram Strait. (2021). Available at: https://doi.org/10.1594/PANGAEA.928251.83.Fadeev, E. edfadeev/Export_and_vert_conn_FRAM: Published workflow. (2021). Available at: https://zenodo.org/record/5515441. More

NEWS AND VIEWS
03 November 2021

A whale of an appetite revealed by analysis of prey consumption

Reaching a deeper understanding of the ocean ecosystems that maintain whales might aid conservation efforts. Measurements of the animals’ krill intake indicate that previous figures were substantial underestimates.

Victor Smetacek

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Victor Smetacek

Victor Smetacek is at the Alfred Wegener Institute Helmholtz Centre for Polar and Marine Research, 27570 Bremerhaven, Germany.

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Baleen whales are the largest known animals that have ever lived. They feed on centimetre-sized prey by filtering seawater through plates of frayed, bristle-like combs, termed baleen, that are fixed to their upper jaws. Previous estimates of the food requirements of whale populations indicate the animals’ enormous food demand1. In the Southern Ocean near Antarctica, before the whaling era, the krill biomass consumed by whales alone is estimated to have been 190 million tonnes annually1, an amount substantially greater than the entire annual world fish catch in modern times2. Intense fishing by humans has decimated ocean fish stocks in a few decades. By contrast, whale feeding seems to be sustainable, as evidenced by hallmarks of the animals’ evolution, such as their long lifespan and high degree of specialization geared to the consumption of just one prey — krill.

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Nature 599, 33-34 (2021)
doi: https://doi.org/10.1038/d41586-021-02951-3

References1.Laws, R. M. Phil. Trans. R. Soc. B 279, 81–96 (1977).Article 

Google Scholar 
2.Pauly, D. & Zeller, D. Nature Commun. 7, 10244 (2016).PubMed 
Article 

Google Scholar 
3.Savoca, M. S. et al. Nature 599, 85–90 (2021).Article 

Google Scholar 
4.Goldbogen, J. A. et al. Science 366, 1367–1372 (2019)PubMed 
Article 

Google Scholar 
5.Williams, T. M. Science 366, 1316–1317 (2019).PubMed 
Article 

Google Scholar 
6.Smetacek, V. in Impacts of Global Warming on Polar Ecosystems (ed. Duarte, C. M.) 45–81 (Fund. BBVA, 2008).
Google Scholar 
7.Nicol, S. et al. Fish Fish. 11, 203–209 (2010).Article 

Google Scholar 
8.Smetacek, V. Protist 169, 791–802 (2018).PubMed 
Article 

Google Scholar 
9.González, H. E. Polar Biol. 12, 81–91 (1992).Article 

Google Scholar 
10.Holm-Hansen, O. & Huntley, M. J. Crustac. Biol. 4 (5), 156–173 (1984).
Google Scholar 
11.Hart, T. J. Discov. Rep. 21, 261–356 (1942).
Google Scholar 
12.Hardy, A. Great Waters: A Voyage of Natural History to Study Whales, Plankton and the Waters of the Southern Ocean (Harper & Row, 1967).
Google Scholar 
13.Bar-On, Y. M., Phillips, R. & Milo, R. Proc. Natl Acad. Sci. USA 115, 6506–6511 (2018).PubMed 
Article 

Google Scholar 
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03 November 2021

A seagrass harbours a nitrogen-fixing bacterial partner

How underwater seagrasses obtain the nitrogen they need has been unclear. Evidence has now emerged of a partnership with a bacterium that might be analogous to the system used by many land plants to gain nitrogen.

Douglas G. Capone

 ORCID: http://orcid.org/0000-0002-3968-736X

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Douglas G. Capone

Douglas G. Capone is in the Department of Biological Sciences, University of Southern California, Los Angeles, California 90089, USA.

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Seagrass meadows are a prominent feature of many shallow coastal areas of the temperate through to the tropical ocean. Seagrasses provide a crucial habitat for invertebrates and juvenile fish, stabilize sediments and buffer the shoreline against erosion1. Moreover, they contribute directly and positively to the ‘blue economy’ of the oceans through their long-term storage of carbon2. Lush and highly productive seagrass beds often thrive in nutrient-deficient waters, and attempts to solve the enigma of how they accomplish this feat have driven considerable research over the years. Writing in Nature, Mohr et al.3 provide crucial evidence indicating that the success of a seagrass called Posidonia oceanica (Fig. 1), which proliferates throughout the warm waters of the Mediterranean Sea (and elsewhere), might be attributed to the development of a highly integrated partnership with a bacterium. This system is reminiscent of those found in some terrestrial plants.

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doi: https://doi.org/10.1038/d41586-021-02956-y

References1.Larkum, A. W. D., Orth, R. J. & Duarte, C. M. (eds) Seagrasses: Biology, Ecology and Conservation (Springer, 2006).
Google Scholar 
2.Lovelock, C. E. & Duarte, C. M. Biol. Lett. 15, 20180781 (2019).PubMed 
Article 

Google Scholar 
3.Mohr, W. et al. Nature https://doi.org/10.1038/s41586-021-04063-4 (2021).Article 

Google Scholar 
4.Thies, J. E. in Principles and Applications of Soil Microbiology 3rd edn (eds Gentry, T. J., Fuhrmann, J. J.& Zuberer, D. A.) 455–487 (Elsevier, 2021).
Google Scholar 
5.Zuberer, D. A. in Principles and Applications of Soil Microbiology 3rd edn (eds Gentry, T. J., Fuhrmann, J. J.& Zuberer, D. A.) 423–453 (Elsevier, 2021).
Google Scholar 
6.Larkum, A. W. D., Waycott, M. & Conran, J. G. in Seagrasses of Australia: Structure, Ecology and Conservation (eds Larkum, A. W. D., Kendrick, G. A. & Ralph, P. J.) 3–29 (Springer, 2018).
Google Scholar 
7.Welsh, D. T. Ecol. Lett. 3, 58–71 (2000).Article 

Google Scholar 
8.Cramer, M. J., Haghshenas, N., Bagwell, C. E., Matsui, G. Y. & Lovell, C. R. Int. J. Syst. Evol. Microbiol. 61, 1053–1060 (2011).PubMed 
Article 

Google Scholar 
9.Clúa, J., Roda, C., Zanetti, M. E. & Blanco, F. A. Genes 9, 125 (2018).Article 

Google Scholar 
10.Evans, S. M., Griffin, K. J., Blick, R. A. J., Poore, A. G. B. & Vergés, A. PLoS ONE 13, e0190370 (2018).PubMed 
Article 

Google Scholar 
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Etymology‘Candidatus Celerinatantimonas neptuna’ (nep.tu’na L. fem. n.), pertaining to Neptunus (L. masc. n. Neptune), the Roman god of the seas and the Neptune grass, Posidonia oceanica.SamplingA P. oceanica meadow at 8 m water depth and nearby sandy sediments in Fetovaia Bay, Elba, Italy13 were sampled between June 2014 and September 2019; individual sampling months and years are indicated in the sections below and/or in the figures and tables. In May 2017, a P. oceanica meadow at the island of Pianosa, Italy was also sampled. All of the samples were obtained via SCUBA diving.Complete plants of P. oceanica were carefully separated from the meadow by hand and stored in seawater-filled containers until arrival at the shore-based laboratory. Sediment for use in the laboratory-based aquaria was scooped into containers from nearby sandy patches. Seawater was pumped through a hose (placed at about 0.5 m above the P. oceanica meadow) into several 50 l barrels onboard the boat and was later used in the laboratory for the aquarium and the incubation experiments.The sediment within the seagrass meadow was sampled with stainless steel core tubes (length, 50 cm), which were drilled into the sediment by divers, and the cores were briefly stored at 22 °C (ambient temperature, September 2019) in a seawater-filled barrel until further processing at the shore-based laboratory.Porewater nutrient samples were obtained using stainless steel lances41 at intervals of around 10 cm. Water column nutrient samples were obtained from above the seagrass meadow at the start or end of sampling. Nutrient samples were collected in 15 ml or 50 ml centrifuge tubes and were stored in a cooler box until further processing.Nutrient measurementsWater column nutrients were measured during several sampling campaigns as indicated in Extended Data Table 1a. Ammonium (NH4+) concentrations were measured fluorometrically42 in the nearby shore-based laboratory, and the remaining water was frozen (−20 °C) for later analyses of nitrate (NO3−), nitrite (NO2−), phosphate (PO43−) and silicate (SiO44−) using an autoanalyser (QuAAtro, Seal Analytical). Porewater samples were obtained in June 2019 and were processed the same as the water column nutrient samples with the exception that ammonium was not measured on site but at the home laboratory at the same time as the other nutrients. Dissolved inorganic nitrogen (ammonium plus NOx−) concentrations in the porewater were averaged for the upper 20 cm (Extended Data Table 1b).Net primary production measurements using the EC methodNet carbon dioxide (CO2) fluxes were calculated on the basis of oxygen (O2) fluxes determined using the aquatic eddy covariance (EC) method. In this non-invasive approach, turbulence-induced transport is resolved using high-frequency current meters combined with fast O2 microsensors. Under the assumption of stationarity, the instantaneous turbulent flux contributions are calculated by correlating vertical current fluctuations to oxygen fluctuations. Our EC system was equipped with an acoustic Doppler velocimeter (ADV, Nortek) and ultra-fast responding optode microsensors with a tip diameter of 430 µm (t90  More