More stories

  • in

    Declines and recovery in endangered Galapagos pinnipeds during the El Niño event

    1.Baylis, A. M. et al. Disentangling the cause of a catastrophic population decline in a large marine mammal. Ecology 96, 2834–2847 (2015).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    2.Hernández-Camacho, C. & Trites, A. Population viability analysis of Guadalupe fur seals Arctocephalus townsendi. Endanger. Species Res. 37, 255–267 (2018).Article 

    Google Scholar 
    3.Lee, O. A., Burkanov, V. & Neill, W. H. Population trends of northern fur seals (Callorhinus ursinus) from a metapopulation perspective. J. Exp. Mar. Biol. Ecol. 451, 25–34 (2014).Article 

    Google Scholar 
    4.Williams, P. J., Hooten, M. B., Womble, J. N., Esslinger, G. G. & Bower, M. R. Monitoring dynamic spatio-temporal ecological processes optimally. Ecology 99(3), 524–535 (2018).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    5.Wege, M. et al. Trend changes in sympatric Subantarctic and Antarctic fur seal pup populations at Marion Island. Southern Ocean. Mar. Mam. Sci. 32(3), 960–982 (2016).Article 

    Google Scholar 
    6.McIntosh, R. R. et al. Understanding meta-population trends of the Australian fur seal, with insights for adaptive monitoring. PLoS ONE 13(9), e0200253. https://doi.org/10.1371/journal.pone.0200253 (2018).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    7.Harwood, J. & Prime, J. H. Some factors affecting the size of British grey seal populations. J. Appl. Ecol. 15, 401–411 (1978).Article 

    Google Scholar 
    8.Trillmich, F. et al. On the challenge of interpreting census data: Insights from a study of an endangered pinniped. PLoS ONE 12(5), e0154588. https://doi.org/10.1371/journal.pone.0154588 (2016).CAS 
    Article 

    Google Scholar 
    9.Taylor, R. H., Barton, K. J., Wilson, P. R., Thomas, B. W. & Karl, B. Population status and breeding of New Zealand fur seals (Arctocephalus forsteri) in the Nelson–northern Marlborough region, 1991–94. New. Zeal. J. Mar. Fresh. 29, 223–234 (1995).Article 

    Google Scholar 
    10.Riofrío-Lazo, M., Arreguín-Sánchez, F. & Páez-Rosas, D. Population abundance of the endangered galapagos Sea Lion Zalophus wollebaeki in the Southeastern galapagos archipelago. PLoS ONE 12(1), e0168829. https://doi.org/10.1371/journal.pone.0168829 (2017).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    11.García-Aguilar, M. C., Elorriaga-Verplancken, F. R., Rosales-Nanduca, H. & Schramm, Y. Population status of the Guadalupe fur seal (Arctocephalus townsendi). J. Mammal. 99(6), 1522–1528 (2018).
    Google Scholar 
    12.Forcada, J., Trathan, P. N., Reid, K. & Murphy, E. J. The effects of global climate variability in pup production of Antarctic fur seals. Ecology 86(9), 2408–2417 (2005).Article 

    Google Scholar 
    13.Taylor, B. L., Martinez, M., Gerrodette, T. & Barlow, J. Lessons from monitoring trends in abundance of marine mammals. Mar. Mam. Sci. 23, 157–175 (2007).Article 

    Google Scholar 
    14.Soto, K. H., Trites, A. W. & Arias-Schreiber, M. The effects of prey availability on pup mortality and the timing of birth of South American sea lions (Otaria flavescens) in Peru. J. Zool. 264, 419–428 (2004).Article 

    Google Scholar 
    15.Elorriaga-Verplancken, F., Sierra-Rodríguez, G., Rosales-Nanduca, H., Acevedo-Whitehouse, K. & Sandoval-Sierra, J. Impact of the 2015 El Niño-Southern Oscillation on the Abundance and Foraging Habits of Guadalupe Fur Seals and California Sea Lions from the San Benito Archipelago. Mexico. PLoS ONE. 11(5), e0155034. https://doi.org/10.1371/journal.pone.0155034 (2016).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    16.Villegas-Amtmann, S., Simmons, S. E., Kuhn, C. E., Huckstadt, L. A. & Costa, D. P. Latitudinal range influences the seasonal variation in the foraging behavior of marine top predators. PLoS ONE 6(8), e23166. https://doi.org/10.1371/journal.pone.0023166 (2011).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    17.Hoskins, A. J., Costa, D. P., Wheatley, K. E., Gibbens, J. R. & Arnould, J. P. Influence of intrinsic variation on foraging behaviour of adult female Australian fur seals. Mar. Ecol. Prog. Ser. 526, 227–239 (2015).ADS 
    Article 

    Google Scholar 
    18.Guinet, C., Jouventin, P. & Georges, J. Y. Long term population changes of fur seals Arctocephalus gazella and Arctocephalus tropicalis on subantarctic (Crozet) and subtropical (St. Paul and Amsterdam) islands and their possible relationship to El Niño southern oscillation. Antarct. Sci. 6(4), 473–478 (1994).19.Chilvers, B. L., Wilkinson, I. S. & Childerhouse, S. New Zealand sea lion, Phocarctos hookeri, pup production 1995 to 2006. New. Zeal. J. Mar. Fresh. 41, 205–213 (2007).Article 

    Google Scholar 
    20.Weise, M. J. & Harvey, J. T. Temporal variability in ocean climate and California sea lion diet and biomass consumption: implications for fisheries management. Mar. Ecol. Prog. Ser. 373, 157–172 (2008).ADS 
    Article 

    Google Scholar 
    21.Robinson, H., Thayer, J., Sydeman, W. J. & Weise, M. J. Changes in California sea lion diet during a period of substantial climate variability. Mar. Biol. 165, 169. https://doi.org/10.1007/s00227-018-3424-x (2018).Article 

    Google Scholar 
    22.Trillmich, F. & Dellinger, T. The Effects of El Niño on Galapagos Pinnipeds. In: Pinnipeds and El Niño. Ecological Studies (Analysis and Synthesis) (eds. Trillmich, F., & Ono, K. A.) 66–74 (Springer, Heidelberg, 1991).23.Churchill, M., Boessenecker, R. & Clementz, M. Colonization of the Southern Hemisphere by fur seals and sea lions (Carnivora: otariidae), revealed by combined evidence phylogenetic and Bayesian biogeographic analysis. Zool. J. Linn. Soc. 172, 200–225 (2014).Article 

    Google Scholar 
    24.Páez-Rosas, D., Aurioles-Gamboa, D., Alava, J. J. & Palacios, D. Stable isotopes indicate differing foraging strategies in two sympatric otariids of the Galapagos Islands. J. Exp. Mar. Bio. Ecol. 425, 44–52 (2012).Article 
    CAS 

    Google Scholar 
    25.Villegas-Amtmann, S., Jeglinski, J. W. E., Costa, D. P., Robinson, P. W. & Trillmich, F. Individual foraging strategies reveal niche overlap between endangered Galapagos Pinnipeds. PLoS ONE 8(8), e70748. https://doi.org/10.1371/journal.pone.0070748 (2013).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    26.Alava, J. J. & Salazar, S. Status and conservation of otariids in Ecuador and the Galapagos Islands. In: Sea lions of the world (eds. Trites, A. W., et al.) 495–519 (Fairbanks, 2006).27.Trillmich, F. Zalophus wollebaeki: The IUCN Red List of Threatened Species. e.T41668A45230540; https://dx.doi.org/https://doi.org/10.2305/IUCN.UK.2015-2.RLTS.T41668A45230540.en (2015).28.Trillmich, F. Arctocephalus galapagoensis. The IUCN Red List of Threatened Species. e.T2057A45223722; https://dx.doi.org/https://doi.org/10.2305/IUCN.UK.2015-2.RLTS.T2057A45223722.en (2015).29.Páez-Rosas, D. & Guevara, N. Management strategies and conservation status of Galapagos sea lion populations at San Cristóbal Island, Galapagos, Ecuador. In: Tropical Pinnipeds: Bio- Ecology, Threats and Conservation (ed. Alava, J. J.) 159–175 (Taylor & Francis Group, Abingdon, 2017).30.Trillmich, F. Galapagos sea lions and fur seals. Noticias de Galápagos. 29, 8–14 (1979).
    Google Scholar 
    31.Wolf, J. B. et al. Tracing early stages of species differentiation: Ecological, morphological and genetic divergence of Galápagos sea lion populations. BMC Evol. Biol. 8, 150. https://doi.org/10.1186/1471-2148-8-150 (2008).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    32.Palacios, D. Seasonal patterns of sea surface temperature and ocean color around the Galapagos: regional and local influences. Deep Sea Res. Part II Top. Stud. Oceanogr. 51, 43–57 (2004).33.Palacios, D., Bograd, S., Foley, D. & Schwing, F. Oceanographic characteristics of biological hot spots in the North Pacific: A remote sensing perspective. Deep Sea Res. Part II Top. Stud. Oceanogr. 53(3), 250–269 (2006).34.Schaeffer, B. et al. Phytoplankton biomass distribution and identification of productive habitats within the Galapagos Marine Reserve by MODIS, a surface acquisition system. Remote Sens. Environ. 112(6), 3044–3054 (2008).ADS 
    Article 

    Google Scholar 
    35.Trillmich, F. & Wolf, J. B. Parent-offspring and sibling conflict in Galapagos fur seals and sea lions. Behav. Ecol. Sociobiol. 62, 363–375 (2008).Article 

    Google Scholar 
    36.Mueller, B., Pörschmann, U., Wolf, J. B. & Trillmich, F. Growth under uncertainty: the influence of marine variability on early development of Galapagos sea lions. Mar. Mam. Sci. 27, 350–365 (2011).Article 

    Google Scholar 
    37.Bonnell, M. L. & Ford, R. G. California sea lion distribution: a statistical analysis of aerial transect data. J. Wildl. Manage. 51, 13–20 (1987).Article 

    Google Scholar 
    38.Edgar, G. J. et al. Conservation of threatened species in the Galapagos Marine Reserve through identification and protection of marine key biodiversity areas. Aqua. Conserv. Mar. Freshw. Ecosyst. 18, 955–968 (2008).Article 

    Google Scholar 
    39.Edgar, G. J., Banks, S., Fariña, J. M., Calvopiña, M. & Martínez, C. Regional biogeography of shallow reef fish and macro-invertebrate communities in the Galapagos archipelago. J. Biogeogr. 31, 1107–1124 (2004).Article 

    Google Scholar 
    40.Ruttenberg, B. I., Haupt, A. J., Chiriboga, A. I. & Warner, R. R. Patterns, causes and consequences of regional variation in the ecology and life history of a reef fish. Oecologia 145, 394–403 (2005).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    41.Wellington, G. M., Strong, A. E. & Merlen, G. Sea surface temperature variation in the Galápagos Archipelago: a comparison between AVHRR nighttime satellite data and in-situ instrumentation (1982–1988). Bull. Mar. Res. 69, 27–42 (2001).
    Google Scholar 
    42.Le Boeuf, B. J. et al. Size and distribution of the California sea lion population in Mexico. Proc. Calif. Acad. Sci. 43, 77–85 (1983).
    Google Scholar 
    43.Fielder, P. C. & Talley, L. D. Hydrography of the tropical Eastern Pacific: a review. Prog. In Ocean. 69, 143–180 (2006).ADS 
    Article 

    Google Scholar 
    44.Brand, L. E., Guillard, R. R. & Murphy, L. S. A method for therapid and precise determination of acclimated phytoplankton reproduction rates. J. Plankton. Res. 3, 193–201 (1981).Article 

    Google Scholar 
    45.Riedman, M. The Pinnipeds: seals, sea lions and walruses (University of California Press, 1990).Book 

    Google Scholar 
    46.Costa, D. P., Weise, M. J. & Arnould, J. P. Potential influences of whaling on the status and trends of pinniped populations (University of California Press, 2006).
    Google Scholar 
    47.Kalberer, S., Meise, K., Trillmich, F. & Krüger, O. Reproductive performance of a tropical apex predator in an unpredictable habitat. Behav. Ecol. Sociobiol. 72, 108. https://doi.org/10.1007/s00265-018-2521-7 (2018).Article 

    Google Scholar 
    48.Trillmich, F. & Limberger, D. Drastic effects of El Niño on Galapagos pinnipeds. Oecologia 67(1), 19–22 (1985).ADS 
    PubMed 
    Article 

    Google Scholar 
    49.Cai, W. et al. Increasing frequency of extreme El Niño events due to greenhouse warming. Nat. Clim. Change. 4, 111–116 (2014).ADS 
    Article 

    Google Scholar 
    50.Wang, G., et al. Continued increase of extreme El Niño frequency long after 1.5 C warming stabilization. Nat. Clim. Change. 7, 568–572 (2017).51.Páez-Rosas, D., Rodríguez-Pérez, M. & Riofrío-Lazo, M. Competition influence in the segregation of the trophic niche of otariids: a case study using isotopic bayesian mixing models in Galapagos pinnipeds. Rapid Commun. Mass Spectrom. 28, 2550–2558 (2014).ADS 
    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    52.Jeglinski, J. W. E., Wolf, J. B., Werner, C., Costa, D. & Trillmich, F. Differences in foraging ecology align with genetically divergent ecotypes of a highly mobile marine top predator. Oecologia 179, 1041–1052 (2015).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    53.Páez-Rosas, D. & Aurioles-Gamboa, D. Spatial variation in the foraging behaviour of the Galapagos sea lions (Zalophus wollebaeki) assessed using scat collections and stable isotope analysis. J. Mar. Biol. Assoc. U.K. 94, 1099–1107 (2014).54.Drago, M. et al. Stable Isotopes Reveal Long-Term Fidelity to Foraging Grounds in the Galapagos Sea Lion (Zalophus wollebaeki). PLoS ONE 11(1), e0147857. https://doi.org/10.1371/journal.pone.0147857 (2016).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    55.Páez-Rosas, D., Villegas-Amtmann, S. & Costa, D. P. Intraspecific variation in feeding strategies of Galapagos sea lions: A case of trophic specialization. PLoS ONE 12(10), e0185165. https://doi.org/10.1371/journal.pone.0185165 (2017).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    56.Villegas-Amtmann, S., McDonald, B., Páez-Rosas, D., Aurioles-Gamboa, D. & Costa, D. P. Adapted to change: Low energy requirements in a low and unpredictable productivity environment, the case of the Galapagos sea lion. Deep Sea Res. Part II Top. Stud. Oceanogr. 140, 94–104 (2017).57.Heller, E. Mammals of the Galapagos Archipelago: Exclusive of the Cetacea (University of Harvard Press, 1904).58.Franco-Trecu, V., Aurioles-Gamboa, D., Arim, M. & Lima, M. Pre-partum and postpartum trophic segregation between sympatrically breeding female Arctocephalus australis and Otaria flavenscens. J. Mammal. 93(2), 514–521 (2012).Article 

    Google Scholar 
    59.Trillmich, F. & Kooyman, G. L. Field metabolic rate of lactating female Galapagos fur seals (Arctocephalus galapagoensis): the influence of offspring age and environment. Comp. Biochem. Phys. A. 129(4), 741–749 (2001).CAS 
    Article 

    Google Scholar 
    60.Lopes, F. et al. Fine-scale matrilineal population structure in the Galapagos fur seal and its implications for conservation management. Conserv. Genet. 16, 1099–1113 (2015).Article 

    Google Scholar 
    61.Jeglinski, J. W. E., Goetz, K. T., Werner, C., Costa, D. P. & Trillmich, F. Same size–same niche? Foraging niche separation between sympatric juvenile Galapagos sea lions and adult Galapagos fur seals. J. Anim. Ecol. 82, 694–706 (2013).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    62.Lowry, L. F., Frost, K. J., Davis, R., DeMaster, D. P. & Suydam, R. S. Movements and behavior of satellite-tagged spotted seals (Phoca largha) in the Bering and Chukchi Seas. Polar Biol. 19, 221–230 (1998).Article 

    Google Scholar 
    63.O’Corry-Crowe, G., Gelatt, T., Rea, L., Bonin, C. & Rehberg, M. Crossing to safety: dispersal, colonization and mate choice in evolutionarily distinct populations of Steller sea lions. Eumetopias jubatus. Mol. Ecol. 23, 5415–5434 (2014).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    64.Forcada, J., Trathan, P. N. & Murphy, E. J. Life history buffering in Antarctic mammals and birds against changing patterns of climate and environmental variation. Glob. Chang. Biol. 14, 2473–2488 (2008).ADS 
    Article 

    Google Scholar 
    65.Pacifici, M. et al. Generation length for mammals. Nat. Conserv. 5, 87–94 (2013).
    Google Scholar 
    66.Dellinger, T. & Trillmich, F. Fish prey of the sympatric Galapagos fur seals and sea lions: seasonal variation and niche separation. Can. J. Zool. 77, 1204–1216 (1999).Article 

    Google Scholar 
    67.Trillmich, F. Attendance behavior of Galapagos sea lions. In: Fur Seals: Maternal Strategies on Land and at Sea. (eds. Gentry, R. L. & Kooyman, G. L.) 196–208 (Princeton University Press, 1986).68.Trillmich, F. Maternal investment and sex-allocation in the Galapagos fur seal. Arctocephalus galapagoensis. Behav. Ecol. Sociobiol. 19(3), 157–164 (1986).
    Google Scholar 
    69.Riofrío-Lazo, M. & Páez-Rosas, D. Galapagos sea lions and fur seals: adaptations to environmental variability. In: Ethology and Behavioral Ecology of Otariids and the Odobenid (eds. Campagna, C. & Harcourt, R.) (Springer Science & Business Media, Germany, 2021).70.Adame, F., Elorriaga-Verplancken, F., Beier, E., Acevedo-Whitehouse, K. & Pardo, M. The demographic decline of a sea lion population followed multi-decadal sea surface warming. Sci. Rep. 10, 10499. https://doi.org/10.1038/s41598-020-67534-0 (2020).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    71.García-Aguilar, M. C., Turrent, C., Elorriaga-Verplancken, F. R., Arias-Del-Razo, A. & Schramm, Y. Climate change and the northern elephant seal (Mirounga angustirostris) population in Baja California. Mexico. PLoS ONE. 13(2), e0193211. https://doi.org/10.1371/journal.pone.0193211 (2018).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    72.Mueller, B., Porschmann, U., Wolf, J. B. W. & Trillmich, F. Growth under uncertainty: the influence of marine variability on early development of Galapagos sea lions. Mar. Mammal. Sci. 27, 350–365 (2011).Article 

    Google Scholar 
    73.Doney, S. C. et al. Climate change impacts on marine ecosystems. Ann. Rev. Mar. Sci. 4, 11–37 (2011).Article 

    Google Scholar 
    74.Wernberg, T. et al. An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot. Nat. Clim. Change. 3, 78–82 (2013).ADS 
    Article 

    Google Scholar 
    75.Páez-Rosas, D., Moreno-Sánchez, X., Tripp-Valdez, A., Elorriaga-Verplancken, F. & Carranco-Narváez, S. Changes in the Galapagos sea lion diet as a response to El Niño-Southern Oscillation. Reg. Stud. Mar. Sci. 40, 101485. https://doi.org/10.1016/j.rsma.2020.101485 (2020).Article 

    Google Scholar 
    76.Urquía, D. & Páez-Rosas, D. δ13C and δ15N values in pup whiskers as a proxy for the trophic behavior of Galapagos sea lion females. Mamm. Biol. 96, 28–36 (2019).Article 

    Google Scholar 
    77.Martin, J. H. et al. Testing the iron hypothesis in ecosystems of the equatorial Pacific-Ocean. Nature 371(6493), 123–129 (1994).ADS 
    CAS 
    Article 

    Google Scholar 
    78.Sakamoto, C.M., et al. Surface seawater distributions of inorganic carbon and nutrients around the Galapagos Islands: results from the PlumEx experiment using automated chemical mapping. Deep Sea Res. Part 2 Top Stud. Oceanogr. 45(6), 1055–1071 (1998).79.Fritz, L. W. & Hinckley, S. A. Critical review of the regime shift “junk food” nutritional stress hypothesis for the decline of the western stock of Steller sea lion. Mar. Mammal. Sci. 21, 476–518 (2005).Article 

    Google Scholar 
    80.McClatchie, S. et al. Food limitation of sea lion pups and the decline of forage off central and southern California. R. Soc. Open Sci. 3, 150628. https://doi.org/10.1098/rsos.150628 (2016).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    81.Villegas-Amtmann, S., Costa, D., Tremblay, Y., Aurioles-Gamboa, D. & Salazar, S. Multiple foraging strategies in a marine apex predator, the Galapagos Sea Lion. Mar. Ecol. Prog. Ser. 363, 299–309 (2008).ADS 
    Article 

    Google Scholar 
    82.Kraus, C. et al. Mama’s boy: sex differences in juvenile survival in a highly dimorphic large mammal, the Galapagos sea lion. Oecologia 171, 893–903 (2013).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    83.Gentry, R. L. & Kooyman, G. L. Fur seals: Maternal Strategies on Land and at Sea (Princeton University Press, 1987). More

  • in

    Diet and trophic niche of the invasive signal crayfish in the first invaded Italian stream ecosystem

    1.Holdich, D. M. M., Reynolds, J. D. D., Souty-Grosset, C. & Sibley, P. J. J. A review of the ever increasing threat to European crayfish from non- indigenous crayfish species. Knowl. Manag. Aquat. Ecosyst. 11, 394–395 (2009).
    Google Scholar 
    2.Kouba, A., Petrusek, A. & Kozák, P. Continental-wide distribution of crayfish species in Europe: Update and maps. Knowl. Manag. Aquat. Ecosyst. 05, 413 (2014).
    Google Scholar 
    3.Edgerton, B. F. et al. Understanding the causes of disease in European freshwater crayfish. Conserv. Biol. 18, 1466–1474 (2004).Article 

    Google Scholar 
    4.Jussila, J., Vrezec, A., Makkonen, J., Kortet, R. & Kokko, H. Invasive crayfish and their invasive diseases in Europe with the focus on the virulence evolution of the crayfish plague invasive crayfish and their invasive diseases. In Biological Invasions in Changing Ecosystems (ed. Canning-Clode, J.) 183–204 (De Gruyter Open Ltd, 2015).
    Google Scholar 
    5.Nyström, P. Ecological impact of introduced and native crayfish on freshwater communities: European perspectives. In Crayfish in Europe as Alien Species – How to Make the Best of Bad Situation? (eds Gherardi, F. & Holdich, D. M.) 63–85 (Rotterdam, 1999).
    Google Scholar 
    6.McCarthy, J.M., Hein, C.L., Olden, J.D. & Vander Zanden, M.J. Coupling long-term studies with meta-analysis to investigate impacts of non-native crayfish on zoobenthic communities. Freshw. Biol. 51, 224–235 (2006).7.Twardochleb, L. A., Julian, D. & Larson, E. R. A global meta-analysis of the ecological impacts of nonnative crayfish. Fresh. Sci. 4, 1367–1382 (2013).Article 

    Google Scholar 
    8.Galib, S. M., Findlay, J. S. & Lucas, M. C. Strong impacts of signal crayfish invasion on upland stream fish and invertebrate communities. Freshw. Biol. 66, 223–240 (2021).Article 

    Google Scholar 
    9.Rosenthal, S.K., Stevens, S.S. & Lodge, D.M. Whole-lake effects of invasive crayfish (Orconectes spp.) and the potential for restoration. Can. J. Fish. Aquat. Sci. 63, 1276–1285 (2006).10.Parkyn, S. M., Collier, K. J. & Hicks, B. J. New Zealand stream crayfish: functional omnivores but trophic predators?. Freshw. Biol. 46, 641–652 (2001).Article 

    Google Scholar 
    11.Stenroth, P. et al. Stable isotopes as an indicator of diet in omnivorous crayfish (Pacifastacus leniusculus): The influence of tissue, sample treatment, and season. Can. J. Fish. Aquat. Sci. 63, 821–831 (2006).CAS 
    Article 

    Google Scholar 
    12.Correia, A. M. Food choice by the introduced crayfish Procambarus clarkii food choice by the introduced crayfish Procambarus clarkii. Ann. Zool. Fenn. 40, 517–528 (2014).
    Google Scholar 
    13.Abrahamsson, S. A. Dynamics of an isolated population of the crayfish, Astacus astacus Linneo. Oikos 17, 96–107 (1966).Article 

    Google Scholar 
    14.France, R. Ontogenetic shift in crayfish δ13C as a measure of land-water ecotonal coupling. Oecologia 107, 239–242 (1996).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    15.Guan, R. Z. & Wiles, P. R. Feeding ecology of the signal crayfish Pacifastacus leniusculus in a British lowland river. Aquaculture 169, 177–193 (1998).Article 

    Google Scholar 
    16.Hanson, J. M., Chambers, P. A. & Prepas, E. E. Selective foraging by the crayfish Orconectes virilis and its impact on macroinvertebrates. Freshw. Biol. 24, 69–80 (1990).Article 

    Google Scholar 
    17.Chambers, P. A., Hanson, J. M., Burke, J. M. & Prepas, E. E. The impact of the crayfish Orconectes virilis on aquatic macrophytes. Freshw. Biol. 24, 81–91 (1990).Article 

    Google Scholar 
    18.Usio, N. & Townsend, C. R. Functional significance of crayfish in stream food webs : Roles of omnivory, substrate heterogeneity and sex. Oikos 98, 512–522 (2002).Article 

    Google Scholar 
    19.Bondar, C. A., Bottriell, K., Zeron, K. & Richardson, J. S. Does trophic position of the omnivorous signal crayfish (Pacifastacus leniusculus) in a stream food web vary with life history stage or density?. Can. J. Fish. Aquat. Sci. 62, 2632–2639 (2005).Article 

    Google Scholar 
    20.Dekar, M. P., Magoulick, D. D. & Huxel, G. R. Shifts in the trophic base of intermittent stream food webs. Hydrobiologia 635, 263–277 (2009).CAS 
    Article 

    Google Scholar 
    21.Evans-White, M. A., Dodds, W. K. & Whiles, M. R. Ecosystem significance of crayfishes and stonerollers in a prairie stream: Functional differences between co-occurring omnivores. J. N. Am. Benthol. Soc. 22, 423–441 (2003).Article 

    Google Scholar 
    22.Machino, Y. Présence de l’écrevisse de Californie (Pacifastacus leniusculus) en Italie. L’Astaciculteur France 52, 2–5 (1997).
    Google Scholar 
    23.Capurro, M. et al. The signal crayfish, Pacifastacus leniusculus (Dana, 1852) [Crustacea: Decapoda: Astacidae], in the Brugneto Lake (Liguria, NW Italy). The beginning of the invasion of the River Po watershed? Aquat. Invas. 2, 17–24 (2007).24.Candiotto, A., Delmastro, G. B., Dotti, L. & Sindaco, R. Pacifastacus leniusculus (Dana, 1852), un nuovo gambero esotico naturalizzato in Piemonte (Crustacea, Decapoda, Astacidae). Riv. Piemontese Storia Nat. 31, 73–82 (2010).
    Google Scholar 
    25.Ghia, D. et al. Distribuzione e naturalizzazione del gambero invasivo Pacifastacus leniusculus nel torrente Valla (Italia nord-occidentale). Ital. J. Freshw. Ichthyol. 4, 101–108 (2017).
    Google Scholar 
    26.Füreder, L. et al. Austropotamobius pallipes. In The IUCN Red List of Threatened Species 2010: e.T2430A9438817 (2010).27.Almeida, D., Ellis, A., England, J. & Copp, G. H. Time-series analysis of native and non-native crayfish dynamics in the Thames River Basin (south-eastern England). Aquat. Conserv. Mar. Freshw. Ecosyst. 24, 192–202 (2014).Article 

    Google Scholar 
    28.Westman, K., Savolainen, R. & Julkunen, M. Replacement of the native crayfish Astacus astacus by the introduced species Pacifastacus leniusculus in a small, enclosed Finnish lake: A 30-year study. Ecography 25, 53–73 (2002).Article 

    Google Scholar 
    29.Ghia, D. et al. Il gambero autoctono italiano e il gambero della California coesistono in un tratto del torrente Valla (Italia nord-occidentale). Ital. J. Freshw. Ichthyol. 5, 120–131 (2018).
    Google Scholar 
    30.Ruokonen, T. J. et al. Introduced alien signal crayfish (Pacifastacus leniusculus) in Finland—Uncontrollable expansion despite numerous crayfisheries strategies. Knowl. Manag. Aquat. Ecosyst. 419, 27 (2018).Article 

    Google Scholar 
    31.Kouba, A., Buric, M. & Petrusek, A. Crayfish species in Europe. In Crayfish Biology and Culture (ed. Kozák, P. et al.) 79–163 (University of South Bohemia in Ceske Budejovice, Faculty of Fisheries and protection of Waters, 2015).32.Ercoli, F., Ruokonen, T. J., Hämäläinen, H. & Jones, R. I. Does the introduced signal crayfish occupy an equivalent trophic niche to the lost native noble crayfish in boreal lakes?. Biol. Invasions 16, 2025–2036 (2014).Article 

    Google Scholar 
    33.Olsson, K., Stenroth, P., Nyström, P. & Graneli, W. Invasions and niche width: Does niche width of an introduced crayfish differ from a native crayfish?. Freshw. Biol. 54, 1731–1740 (2009).Article 

    Google Scholar 
    34.Chucholl, C. Understanding invasion success : Life-history traits and feeding habits of the alien crayfish Orconectes immunis (Decapoda, Astacida, Cambaridae). Knowl. Manag. Aquat. Ecosyst. 404, 04 (2012).Article 

    Google Scholar 
    35.Nakata, K. & Goshima, S. Competition for shelter of preferred sizes between the native crayfish species Cambaroides japonicus and the alien crayfish species Pacifastacus leniusculus in Japan in relation to prior residence, sex difference, and body size. J. Crustac Biol. 23, 897–907 (2003).Article 

    Google Scholar 
    36.Alcorlo, P., Geiger, W. & Otero, M. Feeding preferences and food selection of the red swamp crayfish, Procambarus clarkii, in habitat differing in food item diversity. Crustaceana 77, 435–453. https://doi.org/10.1163/1568540041643283 (2004).Article 

    Google Scholar 
    37.Bondar, C. & Richardson, J. S. Effects of ontogenetic stage and density on the ecological role of the signal crayfish (Pacifastacus leniusculus ) in a coastal Pacific stream. J. N. Am. Benthol. Soc. 28, 294–304 (2009).Article 

    Google Scholar 
    38.Usio, N., Kamiyama, R., Saji, A. & Takamura, N. Size-dependent impacts of invasive alien crayfish on a littoral marsh community. Biol. Conserv. 142, 1480–1490 (2009).Article 

    Google Scholar 
    39.Whitledge, G. W. & Rabeni, C. F. Energy sources and ecological role of crayfishes in an Ozark stream: Insights from stable isotopes and gut analysis. Can. J. Fish. Aquat. Sci. 54, 2555–2563 (1997).Article 

    Google Scholar 
    40.Momot, W. T. Redefining the role of crayfish in aquatic ecosystems. Rev. Fish. Sci. https://doi.org/10.1080/10641269509388566 (1995).Article 

    Google Scholar 
    41.Nyström, P., Brönmark, C. & Granéli, W. Patterns in benthic food webs: A role for omnivorous crayfish?. Freshw. Biol. 36, 631–646 (1996).Article 

    Google Scholar 
    42.Stites, A. J., Taylor, C. A. & Kessler, E. J. Trophic ecology of the North American crayfish genus Barbicambarus Hobbs, 1969 (Decapoda: Astacoidea: Cambaridae): Evidence for a unique relationship between body size and trophic position. J. Crustacean Biol. 37, 263–271 (2017).Article 

    Google Scholar 
    43.Correia, A.M. & Anastácio, P.M. Shifts in aquatic macroinvertebrate biodiversity associated with the presence and size of an alien crayfish. Ecol. Res. 23, 729–734 (2008).44.Johnson, M. F., Rice, S. P. & Reid, I. The activity of signal crayfish (Pacifastacus leniusculus) in relation to thermal and hydraulic dynamics of an alluvial stream, UK. Hydrobiologia 724, 41–54 (2014).Article 

    Google Scholar 
    45.Guan, R. Z. Abundance and production of the introduced signal crayfish in a British lowland river. Aquac. Int. 8, 59–76 (2000).Article 

    Google Scholar 
    46.Almeida, D. et al. Environmental biology of an invasive population of signal crayfish in the River Stort catchment (southeastern England). Limnologica 43, 177–184 (2013).Article 

    Google Scholar 
    47.Hein, C.L., Roth, B.M., Ives, A.R. & Vander Zanden, M.J. Fish predation and trapping for rusty crayfish (Orconectes rusticus) control: A whole-lake experiment. Can. J. Fish. Aquat. Sci. 63, 383–393 (2006).48.Houghton, R. J., Wood, C. & Lambin, X. Size-mediated, density-dependent cannibalism in the signal crayfish Pacifastacus leniusculus (Dana, 1852) (Decapoda, Astacidea), an invasive crayfish in Britain. Crustaceana 90, 417–435 (2017).Article 

    Google Scholar 
    49.Bondar, C. A. & Richardson, J. S. Stage-specific interactions between dominant consumers within a small stream ecosystem: Direct and indirect consequences. Freshw. Sci. 32, 183–192 (2013).Article 

    Google Scholar 
    50.Nyström, P. Ecology. In Biology of Freshwater Crayfish (ed. Holdich, D.M.) 192–235 (Blackwel Science, 2002).51.Gherardi, F., Acquistapace, P. & Santini G. Food selection in freshwater omnivores: A case study of crayfish Austropotamobius pallipes. Arch. Hydrobiol.159, 357–376 (2004).52.Moorhouse, T. P. et al. Intensive removal of signal crayfish (Pacifastacus leniusculus) from rivers increases numbers and taxon richness of macroinvertebrate species. Ecol. Evol. https://doi.org/10.1002/ece3.903 (2014).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    53.Ishikawa, N. F., Doi, H. & Finlay, J. C. Global dataset for carbon and nitrogen stable isotope ratios of lotic periphyton. Ecol. Res. 33, 1089 (2018).CAS 
    Article 

    Google Scholar 
    54.Westman, K., Savolainen, R. & Pursiainen, M. Development of the introduced North American signal crayfish, Pacifastacus leniusculus (Dana), population in a small Finnish forest lake in 1970–1997. Boreal Environ. Res. 4, 387–407 (1999).
    Google Scholar 
    55.Stewart, K. W. & Stark, B. P. Nymphs of North American Stonefly Genera (Plecoptera) (The Caddis Press, 2002).
    Google Scholar 
    56.Bo, T., Cammarata, M., Candiotto, A. & Fenoglio, S. Trophic preferences of three allochthonous fishes in Bormida River (Alessandria, NW Italy). Hidrobiologica 22, 195–200 (2012).
    Google Scholar 
    57.Jackson, A. L., Inger, R., Parnell, A. C. & Bearhop, S. Comparing isotopic niche widths among and within communities: SIBER-stable isotope Bayesian ellipses in R. J. Anim. Ecol. 80, 595–602 (2011).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    58.R Development Core Team. R: A Language and Environment for Statistical Computing. http://www.R-project.org (R Foundation for Statistical Computing, 2016).59.Jackson, A.L. Ellipse Overlap. https://cran.rproject.org/web/packages/SIBER/vignettes/Ellipse-Overlap.html (2020).60.Stock, B. C. & Semmens, B. X. MixSIAR GUI user manual version 31, 1–42. https://doi.org/10.5281/zenodo.47719 (2016).Article 

    Google Scholar 
    61.Stock, B. C. et al. Analyzing mixing systems using a new generation of Bayesian tracer mixing models. PeerJ 6, e5096. https://doi.org/10.7717/peerj.5096 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    62.Stock, B. C. & Semmens, B. X. Unifying error structures in commonly used biotracer mixing models. Ecology 97, 2562–2569 (2016).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    63.Carolan, J. V., Mazumder, D., Dimovski, C., Diocares, R. & Twining, J. Biokinetics and discrimination factors for δ13C and δ15N in the omnivorous freshwater crustacean, Cheraxdestructor. Mar. Freshw. Res. 63, 878–886. https://doi.org/10.1071/MF11240 (2012).CAS 
    Article 

    Google Scholar 
    64.Jussila, J. et al. It takes time to see the menu from the body: An experiment on stable isotope composition in freshwater crayfishes. Knowl. Manag. Aquat. Ecosyst. 416, 25. https://doi.org/10.1051/kmae/2015021 (2015).Article 

    Google Scholar 
    65.Glon, M.G., Larson, E.R. & Pangle, K.L. Comparison of 13C and 15N discrimination factors and turnover rates between congeneric crayfish Orconectes rusticus and O. virilis (Decapoda, Cambaridae). Hydrobiologia 768, 51–61. https://doi.org/10.1007/s10750-015-2527-3 (2016). 66.Vander Zanden, M.J. & Rasmussen, J.B. Variation in delta N-15 and delta C-13 trophic fractionation: Implication for aquatic food web studies. Limnol. Oceanogr. 46, 2061–2066 (2001).67.McCutchan, J. H. Jr., Lewis, W. M., Kendal, C. & McGrath, C. C. Variation in trophic shift for stable isotope ratios of carbon, nitrogen and suphur. Oikos 102, 378–390 (2003).CAS 
    Article 

    Google Scholar  More

  • in

    Division of labor in work shifts by leaf-cutting ants

    1.Roces, F. Individual complexity and self-organization in foraging by leaf-cutting ants. Biol. Bull. 202, 306–313 (2002).PubMed 
    Article 

    Google Scholar 
    2.Cerdá, X., Angulo, E., Boulay, R. & Lenoir, A. Individual and collective foraging decisions: A field study of worker recruitment in the gypsy ant Aphaenogaster senilis. Behav. Ecol. Sociobiol. 63, 551–562 (2009).Article 

    Google Scholar 
    3.Dussutour, A., Deneubourg, J.-L., Beshers, S. & Fourcassié, V. Individual and collective problem-solving in a foraging context in the leaf-cutting ant Atta colombica. Anim. Cogn. 12, 21–30 (2009).PubMed 
    Article 

    Google Scholar 
    4.Leboeuf, A. C. & Grozinger, C. M. Me and we: The interplay between individual and group behavioral variation in social collectives. Curr. Opin. Insect Sci. 5, 16–24 (2014).PubMed 
    Article 

    Google Scholar 
    5.Feinerman, O. & Korman, A. Individual versus collective cognition in social insects. J. Exp. Biol. 220, 73–82 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    6.Frank, E. T. & Linsenmair, K. E. Individual versus collective decision making: Optimal foraging in the group-hunting termite specialist Megaponera analis. Anim. Behav. 130, 27–35 (2017).Article 

    Google Scholar 
    7.Menzel, R., Leboulle, G. & Eisenhardt, D. Small brains, bright minds. Cell 124, 237–239 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    8.Leadbeater, E. & Chittka, L. Social learning in insects—From miniature brains to consensus building. Curr. Biol. 17, 703–713 (2007).Article 
    CAS 

    Google Scholar 
    9.Giurfa, M. Cognition with few neurons: Higher-order learning in insects. Trends Neurosci. 36, 285–294 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    10.Guerrieri, F. J. & D’Ettorre, P. Associative learning in ants: Conditioning of the maxilla-labium extension response in Camponotus aethiops. J. Insect Physiol. 56, 88–92 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    11.Gordon, D. M. The dynamics of the daily round of the harvester ant colony (Pogonomyrmex barbatus). Anim. Behav. 34, 1402–1419 (1986).Article 

    Google Scholar 
    12.Goss, S., Aron, S., Deneubourg, J. L. & Pasteels, J. M. Self-organized shortcuts in the Argentine ant. Naturwissenschaften 76, 579–581 (1989).ADS 
    Article 

    Google Scholar 
    13.Gordon, D. M. The organization of work in social insect colonies. Nature 380, 121–124 (1996).ADS 
    CAS 
    Article 

    Google Scholar 
    14.Czaczkes, T. J. et al. Composite collective decision-making. Proc. Biol. Sci. 282, 20142723 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    15.Bonabeau, E., Theraulaz, G., Deneubourg, J.-L., Aron, S. & Camazine, S. Self-organization in social insects. TREE 12, 188–194 (1997).CAS 
    PubMed 

    Google Scholar 
    16.Boomsma, J. J. & Franks, N. R. Social insects: From selfish genes to self organisation and beyond. Trends Ecol. Evol. 21, 303–308 (2006).PubMed 
    Article 

    Google Scholar 
    17.Camazine, S., Deneubourg, J.L., Franks, N.R., Sneyd, J., Theraulaz, G., Bonabeau, E. Self-Organization in Biological Systems. (Princeton University Press, 2003).18.Constant, N., Santorelli, L.A., Lopes, J.F.S., Hughes, W.O.H. The effects of genotype, caste, and age on foraging performance in leaf-cutting ants. Behav. Ecol. 23, 1284–1288 (2012).19.Feinerman, O. & Traniello, J. F. A. Social complexity, diet, and brain evolution: Modeling the effects of colony size, worker size, brain size, and foraging behavior on colony fitness in ants. Behav. Ecol. Sociobiol. 70, 1063–1074 (2016).Article 

    Google Scholar 
    20.McCluskey, E.S. Circadian-rhythms in male-ants of five diverse species. Science (80- ) 150, 1037–1039 (1965).21.North, R. D. Circadian rhythm of locomotor activity in individual workers of the wood ant Formica rufa. Physiol. Entomol. 12, 445–454 (1987).Article 

    Google Scholar 
    22.Cros, S., Cerdá, X., Retana, J., De, E. U. & De, C. F. Spatial and temporal variations in the activity patterns of Mediterranean ant communities. Écoscience 4, 269–278 (1997).Article 

    Google Scholar 
    23.Bellusci, S. & David, M. M. Circadian activity rhythm of the foragers of a eusocial bee (Scaptotrigona aff depilis, Hymenoptera, Apidae, Meliponinae) outside the nest. Biol. Rhythm Res. 32, 117–124 (2001).Article 

    Google Scholar 
    24.Narendra, A., Reid, S.F., Greiner, B., Peters, R.A., Hemmi, J.M., Ribi, W.A. et al. Caste-specific visual adaptations to distinct daily activity schedules in Australian Myrmecia ants. Proc. Biol. Sci. 278, 1141–1149 (2011).25.Yilmaz, A., Aksoy, V., Camlitepe, Y. & Giurfa, M. Eye structure, activity rhythms, and visually-driven behavior are tuned to visual niche in ants. Front. Behav. Neurosci. 8, 205 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    26.Nickele, M. A., Filho, W. R., Pie, M. R. & Penteado, S. R. C. Daily foraging activity of Acromyrmex (Hymenoptera: Formicidae) leaf-cutting ants. Sociobiology 63, 645–650 (2016).Article 

    Google Scholar 
    27.Aschoff, J. Exogenous and endogenous components in circadian rhythms. Cold Spring Harb. Symp. Quant. Biol. 25, 11–28 (1960).CAS 
    PubMed 
    Article 

    Google Scholar 
    28.Hall, J. C. Genetics and molecular biology of rhythms in Drosophila and other insects. Adv. Genet. 48, 1–280 (2003).CAS 
    PubMed 
    Article 

    Google Scholar 
    29.Sandrelli, F., Costa, R., Kyriacou, C. P. & Rosato, E. Comparative analysis of circadian clock genes in insects. Insect Mol. Biol. 17, 447–463 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    30.Hamilton, W. D. The genetical evolution of social behaviour. I. J. Theor. Biol. 7, 1–16 (1964).CAS 
    Article 

    Google Scholar 
    31.Abbot, P., Abe, J., Alcock, J., Alizon, S., Alpedrinha, J.A.C., Andersson, M. et al. Inclusive fitness theory and eusociality. Nature 471, E1–E4 (2011).32.Kost, C., De Oliveira, E. G., Knoch, T. A. & Wirth, R. Spatio-temporal permanence and plasticity of foraging trails in young and mature leaf-cutting ant colonies (Atta spp.). J. Trop. Ecol. 21, 677–688 (2005).33.Bochynek, T., Meyer, B. & Burd, M. Energetics of trail clearing in the leaf-cutter ant Atta. Behav. Ecol. Sociobiol. 71, 1–10 (2017).Article 

    Google Scholar 
    34.Bouchebti, S., Travaglini, R. V., Forti, L. C. & Fourcassié, V. Dynamics of physical trail construction and of trail usage in the leaf-cutting ant Atta laevigata. Ethol. Ecol. Evol. 31, 105–120 (2019).Article 

    Google Scholar 
    35.Cherrett, J. M. The foraging behavior of Atta cephalotes L. J. Anim. Ecol. 37, 387–403 (1968).Article 

    Google Scholar 
    36.Lewis, T., Pollard, G.V., Dibley, G.C. Rhythmic foraging in the leaf-cutting ant Atta cephalotes (L.) (Formicidae: Attini). J. Anim. Ecol. 43, 129 (1974).37.Sharma, V. K., Lone, S. R., Mathew, D., Goel, A. & Chandrashekaran, M. K. Possible evidence for shift work schedules in the media workers of the ant species Camponotus compressus. Chronobiol. Int. 21, 297–308 (2004).PubMed 
    Article 

    Google Scholar 
    38.Koto, A., Mersch, D., Hollis, B. & Keller, L. Social isolation causes mortality by disrupting energy homeostasis in ants. Behav. Ecol. Sociobiol. 69, 583–591 (2015).Article 

    Google Scholar 
    39.Wilson, E.O. Caste and division of labor in leaf-cutter ants (Hymenoptera: Formicidae: Atta) I. The overall pattern in A. sexdens. Behav. Ecol. Sociobiol. 7, 143–156 (1980).40.Wilson, E.O. Caste and division of labor in leaf-cutter ants (Hymenoptera : Formicidae : Atta) II. The ergonomic optimization of leaf cutting. Behav. Ecol. Sociobiol. 7, 157–165 (1980).41.Holbrook, C. T., Eriksson, T. H., Overson, R. P., Gadau, J. & Fewell, J. H. Colony-size effects on task organization in the harvester ant Pogonomyrmex californicus. Insect. Soc. 60, 191–201 (2013).Article 

    Google Scholar 
    42.Martinoya, C., Bloch, S., Ventura, D. F. & Puglia, N. M. Spectral efficiency as measured by ERG in the ant (Atta sexdens rubropilosa). J. Comp. Physiol A 104, 205–210 (1975).Article 

    Google Scholar 
    43.Kaiser, W. Busy bees need rest, too. J. Comp. Physiol. A 163, 565–584 (1988).Article 

    Google Scholar 
    44.Sauer, S., Herrmann, E. & Kaiser, W. Sleep deprivation in honey bees. J. Sleep Res. 13, 145–152 (2004).PubMed 
    Article 

    Google Scholar 
    45.Klein, B. A., Klein, A., Wray, M. K., Mueller, U. G. & Seeley, T. D. Sleep deprivation impairs precision of waggle dance signaling in honey bees. Proc. Natl. Acad. Sci. 107, 22705–22709 (2010).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    46.Mildner, S. & Roces, F. Plasticity of daily behavioral rhythms in foragers and nurses of the ant Camponotus rufipes: Influence of social context and feeding times. PLoS ONE 12, e0169244 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    47.Fujioka, H. et al. Ant circadian activity associated with brood care type. Biol. Lett. 13, 20160743 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    48.Klein, B. A., Olzsowy, K. M., Klein, A., Saunders, K. M. & Seeley, T. D. Caste-dependent sleep of worker honey bees. J. Exp. Biol. 211, 3028–3040 (2008).PubMed 
    Article 

    Google Scholar 
    49.Bloch, G., Toma, D. P. & Robinson, G. E. Behavioral rhythmicity, age, division of labor and period expression in the honey bee brain. J. Biol. Rhythms 16, 444–456 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    50.Bloch, G. The social clock of the honeybee. J. Biol. Rhythms 25, 307–317 (2010).PubMed 
    Article 

    Google Scholar 
    51.Bloch, G., Sullivan, J. P. & Robinson, G. E. Juvenile hormone and circadian locomotor activity in the honey bee Apis mellifera. J. Insect Physiol. 48, 1123–1131 (2002).CAS 
    PubMed 
    Article 

    Google Scholar 
    52.Bernhard Kraus, F., Gerecke, E., Moritz, R.F.A. Shift work has a genetic basis in honeybee pollen foragers (Apis mellifera L.). Behav. Genet. 41, 323–328 (2011).53.Wilson, E.O. Caste and division of labor in leaf-cutter ants (Hymenoptera: Formicidae: Atta) III. Ergonomic resiliency in foraging by A. cephalotes. Behav. Ecol. Sociobiol. 14, 55–60 (1983).54.Detrain, C., Pasteels, J.M. Caste differences in behavioral thresholds as a basis for polyethism during food recruitment in the ant, Pheidole pallidula (Nyl.) (Hymenoptera: Myrmicinae). J. Insect Behav. 4, 157–176 (1991).55.Lighton, J. R. B. & QuinlanJr, M. C. D. H. F. Is bigger better? Water balance in the polymorphic desert harvester ant Messor pergandei. Physiol. Entomol. 19, 325–334 (1994).Article 

    Google Scholar 
    56.Cerdá, X. & Retana, J. Links between worker polymorphism and thermal biology in a thermophilic ant species. Oikos 78, 467 (1997).Article 

    Google Scholar 
    57.Clémencet, J., Cournault, L., Odent, A. & Doums, C. Worker thermal tolerance in the thermophilic ant Cataglyphis cursor (Hymenoptera, Formicidae). Insectes Soc. 57, 11–15 (2010).Article 

    Google Scholar 
    58.Gadagkar, R. The evolution of caste polymorphism in social insects: Genetic release followed by diversifying evolution. J. Genet. 76, 167–179 (1997).Article 

    Google Scholar 
    59.Helms Cahan, S. & Keller, L. Complex hybrid origin of genetic caste determination in harvester ants. Nature 424, 306–309 (2003).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    60.Fjerdingstad, E. J. & Crozier, R. H. The evolution of worker caste diversity in social insects. Am. Nat. 167, 390–400 (2012).Article 

    Google Scholar 
    61.Trible, W. et al. Orco mutagenesis causes loss of antennal lobe glomeruli and impaired social behavior in ants. Cell 170(727–735), e10 (2017).
    Google Scholar 
    62.De, T. M. A. et al. Two castes sizes of leafcutter ants in task partitioning in foraging activity. Ciênc. Rural 46, 1902–1908 (2016).Article 

    Google Scholar 
    63.Sharkey, K. M. & Eastman, C. I. Melatonin phase shifts human circadian rhythms in a placebo-controlled simulated night-work study. Am. J. Physiol. Integr. Comp. Physiol. 282, R454–R463 (2002).CAS 
    Article 

    Google Scholar  More

  • in

    Deep-sea shipwrecks represent island-like ecosystems for marine microbiomes

    1.Anderson RE, Sogin ML, Baross JA. Biogeography and ecology of the rare and abundant microbial lineages in deep-sea hydrothermal vents. FEMS Microbiol Ecol. 2015;91:1–11.Article 

    Google Scholar 
    2.Galand PE, Casamayor EO, Kirchman DL, Lovejoy C. Ecology of the rare microbial biosphere of the Arctic Ocean. Proc Natl Acad Sci USA. 2009;106:22427–32.CAS 
    Article 

    Google Scholar 
    3.Hanson CA, Fuhrman JA, Horner-Devine MC, Martiny JBH. Beyond biogeographic patterns: processes shaping the microbial landscape. Nat Rev Microbiol. 2012;10:497–506.CAS 
    Article 

    Google Scholar 
    4.Lindstrom ES, Langenheder S. Local and regional factors influencing bacterial community assembly. Env Microbiol Rep. 2012;4:1–9.Article 

    Google Scholar 
    5.Martiny JBH, Bohannan BJM, Brown JH, Colwell RK, Fuhrman JA, Green JL, et al. Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol. 2006;4:102–12.CAS 
    Article 

    Google Scholar 
    6.Ramette A, Tiedje JM. Biogeography: an emerging cornerstone for understanding prokaryotic diversity, ecology, and evolution. Micro Ecol. 2007;53:197–207.Article 

    Google Scholar 
    7.Teittinen A, Soininen J. Testing the theory of island biogeography for microorganisms-patterns for spring diatoms. Aquat Micro Ecol. 2015;75:239–50.Article 

    Google Scholar 
    8.Salazar G, Cornejo-Castillo FM, Benitez-Barrios V, Fraile-Nuez E, Alvarez-Salgado XA, Duarte CM, et al. Global diversity and biogeography of deep-sea pelagic prokaryotes. ISME J. 2016;10:596–608.Article 

    Google Scholar 
    9.Longhurst AR. Chapter 1 – Toward an ecological geography of the sea. Ecological Geography of the Sea, 2nd ed. Burlington: Academic Press; 2007. p. 1–17.10.Duchinski K, Moyer CL, Hager K, Fullerton H. Fine-scale biogeography and the inference of ecological interactions among neutrophilic iron-oxidizing Zetaproteobacteria as determined by a rule-based microbial network. Front Microbiol. 2019;10:1–11.Article 

    Google Scholar 
    11.Inagaki F, Nunoura T, Nakagawa S, Teske A, Lever M, Lauer A, et al. Biogeographical distribution and diversity of microbes in methane hydrate-bearing deep marine sediments, on the Pacific Ocean Margin. Proc Natl Acad Sci USA. 2006;103:2815–20.CAS 
    Article 

    Google Scholar 
    12.Ruff SE, Biddle JF, Teske AP, Knittel K, Boetius A, Ramette A. Global dispersion and local diversification of the methane seep microbiome. Proc Natl Acad Sci USA. 2015;112:4015–20.CAS 
    Article 

    Google Scholar 
    13.Meyer KS. Chapter One – Islands in a sea of mud: Insights from terrestrial island theory for community assembly on insular marine substrata. In: Curry BE, editor. Advances in Marine Biology. 76: Cambridge, Massachusetts: Academic Press; 2017. p. 1–40.14.Paul WS, Amy DA, Gregory SB. Expansion of coral communities within the Northern Gulf of Mexico via offshore oil and gas platforms. Mar Ecol Prog Ser. 2004;280:129–43.Article 

    Google Scholar 
    15.Perkol-Finkel S, Benayahu Y. Recruitment of benthic organisms onto a planned artificial reef: shifts in community structure one decade post-deployment. Mar Environ Res. 2005;59:79–99.CAS 
    Article 

    Google Scholar 
    16.Perkol-Finkel S, Shashar N, Barneah O, Ben-David-Zaslow R, Oren U, Reichart T, et al. Fouling reefal communities on artificial reefs: does age matter? Biofouling. 2005;21:127–40.CAS 
    Article 

    Google Scholar 
    17.Svane I, Petersen JK. On the problems of epibioses, fouling and artificial reefs, a review. Mar Ecol. 2001;22:169–88.Article 

    Google Scholar 
    18.Meyer-Kaiser K, Brooke SD, Sweetman A, Wolf M, Young C. Invertebrate communities on historical shipwrecks in the western Atlantic: relation to islands. Mar Ecol Prog Ser. 2017;566:17–29.Article 

    Google Scholar 
    19.Macarthur RH, Wilson EO, Wilson EO. The theory of island biogeography. Revised ed: Princeton, New Jersey: Princeton University Press; 1967.20.Losos JB, Ricklefs RE, MacArthur RH. The theory of island biogeography revisited. Princeton: Princeton University Press; 2010. xvi, 476 p.21.Stieglitz TC. Habitat engineering by decadal-scale bioturbation around shipwrecks on the Great Barrier Reef mid-shelf. Mar Ecol Prog Ser. 2013;477:29–40.Article 

    Google Scholar 
    22.Hamdan LJ, Salerno JL, Reed A, Joye SB, Damour M. The impact of the Deepwater Horizon blowout on historic shipwreck-associated sediment microbiomes in the northern Gulf of Mexico. Sci Rep. 2018;8:9057.Article 

    Google Scholar 
    23.Church R, Warren D, Cullimore R, Johnston L, Schroeder WW, Patterson W, et al. Archaeological and biological analysis of World War II shipwrecks in the Gulf of Mexico: Artifical reef effect in deep water. New Orleans, LA: U.S. Department of the Interior; 2007. Report No.: MMS 2007-015.24.Mugge RL, Brock ML, Salerno JL, Damour M, Church RA, Lee JS, et al. Deep-sea biofilms, historic shipwreck preservation and the Deepwater Horizon spill. Front Marine Sci. 2019;6:1–17.Article 

    Google Scholar 
    25.Comeau AM, Li WK, Tremblay JE, Carmack EC, Lovejoy C. Arctic Ocean microbial community structure before and after the 2007 record sea ice minimum. Plos One. 2011;6:e27492.CAS 
    Article 

    Google Scholar 
    26.Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37:852–7.CAS 
    Article 

    Google Scholar 
    27.Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–3.CAS 
    Article 

    Google Scholar 
    28.Leibold MA, Holyoak M, Mouquet N, Amarasekare P, Chase JM, Hoopes MF, et al. The metacommunity concept: a framework for multi-scale community ecology. Ecol Lett. 2004;7:601–13.Article 

    Google Scholar 
    29.Levin LA, Baco AR, Bowden DA, Colaco A, Cordes EE, Cunha MR, et al. Hydrothermal vents and methane seeps: rethinking the sphere of influence. Front Mar Sci. 2016;3:1–23.Article 

    Google Scholar 
    30.Goffredi SK, Orphan VJ. Bacterial community shifts in taxa and diversity in response to localized organic loading in the deep sea. Environ Microbiol. 2010;12:344–63.CAS 
    Article 

    Google Scholar 
    31.Smith CR, Baco-Taylor A. Ecology of whale falls at the deep-sea floor. Oceanography and marine biology: an annual review. London: Abredeen University Press; 2003.32.Smith C, Baco-Taylor A, Glover A. Faunal succession on replicate deep-sea whale falls: time scales and vent-seep affinities. Cah Biol Mar. 2002;43:293–7.
    Google Scholar 
    33.Grupe BM, Krach ML, Pasulka AL, Maloney JM, Levin LA, Frieder CA. Methane seep ecosystem functions and services from a recently discovered southern California seep. Mar Ecol. 2015;36:91–108.CAS 
    Article 

    Google Scholar 
    34.Harris PT. Shelf and deep-sea sedimentary environments and physical benthic disturbance regimes: a review and synthesis. Mar Geol. 2014;353:169–84.Article 

    Google Scholar 
    35.Damour M, Church R, Warren D, Horrell C, Hamdan LJ. Gulf of Mexico Shipwreck Corrosion, Hydrocarbon Exposure, Microbiology, and Archaeology (GOM-SCHEMA) Project: studying the effects of a major oil spill on submerged cultural resources. In 2015 Society for Historical Archaeology Annual Conference Proceedings; Seattle, WA: Society for Historical Archaeology; 2016. p. 51–61.36.BOEM. Bureau of Ocean Energy Management Data Center BOEM; 2020. https://www.data.boem.gov/.37.BSEE. Bureau of Safety and Environmental Enforcement (BSEE): Gulf of Mexico OCS Region Facts. New Orleans, Louisiana: Bureau of Safety and Environmental Enforcement; 2020.38.Costello MJ, Tsai P, Wong PS, Cheung AKL, Basher Z, Chaudhary C. Marine biogeographic realms and species endemicity. Nat Commun. 2017;8:1057.Article 

    Google Scholar  More

  • in

    Barrier properties of fungal fruit body skins, pileipelles, contribute to protection against water loss

    1.Nobel, P. S. Physicochemical and Environmental Plant Physiology (Academic Press, 2005).
    Google Scholar 
    2.Hsiao, T. C. Plant responses to water stress. Annu. Rev. Plant Physiol. 24, 519–570 (1973).CAS 
    Article 

    Google Scholar 
    3.Schönherr, J. Resistance of plant surfaces to water loss : transport properties of cutin, suberin and associated lipids. In Encyclopedia Plant Physiology, NS Vol. 12B (eds Lange, O. L. et al.) 154–179 (Springer, 1982).
    Google Scholar 
    4.Lendzian, K. J. Gas permeability of plant cuticles: oxygen permeability. Planta 155, 310–315 (1982).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    5.Langenfeld-Heyser, R. Physiological functions of lenticels. In Trees—Contributions to Modern Tree Physiology (eds Rennenberg, H. et al.) 43–56 (Backhuys, 1997).
    Google Scholar 
    6.Riederer, M. & Schreiber, L. Protecting against water loss: analysis of the barrier properties of plant cuticles. J. Exp. Bot. 52, 2023–2032 (2001).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    7.Kerstiens, G. Parameterization, comparison, and validation of models quantifying relative change of cuticular permeability with physicochemical properties of diffusants. J. Exp. Bot. 57, 2525–2533 (2006).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    8.Schönherr, J. Characterization of aqueous pores in plant cuticles and permeation of ionic solutes. J. Exp. Bot. 57, 2471–2491 (2006).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    9.Groh, B., Hübner, C. & Lendzian, K. J. Water and oxygen permeance of phellems isolated from trees: the role of waxes and lenticels. Planta 215, 794–801 (2002).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    10.Lendzian, K. J. Survival strategies of plants during secondary growth: barrier properties of phellems and lenticels towards water, oxygen, and carbon dioxide. J. Exp. Bot. 57, 2535–2546 (2006).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    11.Renault, H. et al. (2017) A phenol-enriched cuticle is ancestral to lignin evolution in land plants. Nat. Commun. 8, 14713 (2017).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    12.Haas, K. Phytochemische und rasterelektronenmikroskopische Untersuchungen zum Oberflächenwachs von Laubmoosen (Bryatae) (Grauer, 1999).
    Google Scholar 
    13.Clémençon, H., Emmett, V. & Emmett, E. E. Cytology and Plectology of the Hymenomycetes (J Cramer, 2012).
    Google Scholar 
    14.Moore, D., Gange, A. C., Gange, E. G. & Boddy, L. Fruit bodies: their production and development in relation to environment. In Ecology of Saprotrophic Basidiomycetes (eds Boddy, L. et al.) 79–103 (Elsevier Academic Press, 2008).
    Google Scholar 
    15.Halbwachs, H., Simmel, J. & Bässler, C. Tales and mysteries of fungal fruiting: how morphological and physiological traits affect a pileate lifestyle. Fungal Biol. Rev. 30, 36–61 (2016).Article 

    Google Scholar 
    16.Sakamoto, Y. Influences of environmental factors on fruiting body induction, development and maturation in mushroom-forming fungi. Fungal Biol. Rev. 32, 236–248 (2018).Article 

    Google Scholar 
    17.Straatsma, G., Ayer, F. & Egli, S. Species richness, abundance, and phenology of fungal fruit bodies over 21 years in a Swiss forest plot. Mycol. Res. 105(5), 515–523 (2001).Article 

    Google Scholar 
    18.Kües, U. & Liu, Y. Fruiting body production in basidiomycetes. Appl. Microbiol. Biotechnol. 54, 141–152 (2000).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    19.Beluhan, S. & Ranogajec, A. Chemical composition and non-volatile components of Croatian wild edible mushrooms. Food Chem. 124, 1076–1082 (2011).CAS 
    Article 

    Google Scholar 
    20.Beecher, T. M., Magan, N. & Burton, K. S. Water potentials and soluble carbohydrate concentrations in tissues of freshly harvested and stored mushrooms (Agaricusbisporus). Postharvest Biol. Technol. 22, 121–131 (2001).CAS 
    Article 

    Google Scholar 
    21.Bonnier G, Mangin L (1884) Recherches sur la respiration et la transpiration des champignons. Ann. Sc. Natur., sér. VI, t. XVII:210–30522.Moser, M. Transpirationsschutz bei höheren Pilzen. Schweizerische Zeitschrift für Pilzkunde 42(4), 50–54 (1964).
    Google Scholar 
    23.Pieschel, E. Über die Transpiration und die Wasserversorgung der Hymenomyceten. Bot. Archiv. VIII, 64–104 (1924).
    Google Scholar 
    24.Seybold, A. Weitere Beiträge zur Transpirationsanalyse. IV. Über die Transpiration der Hutpilze. Planta 16, 518–525 (1932).Article 

    Google Scholar 
    25.Becker, M., Kerstiens, G. & Schönherr, J. Water permeability of plant cuticles: permeance, diffusion and partition coefficients. Trees 1, 54–60 (1986).CAS 
    Article 

    Google Scholar 
    26.Schreiber, L. & Schönherr, J. Water and Solute Permeability of Plant Cuticles. Measurement and Data Analysis (Springer, 2009).
    Google Scholar 
    27.Schönherr, J. & Lendzian, K. J. A simple and inexpensive method of measuring water permeability of isolated plant cuticular membranes. Z Pflanzenphysiol 102, 321–327 (1981).Article 

    Google Scholar 
    28.Weast, R. C. CRC Handbook of Chemistry and Physics: Humidity Constant (CRC Press, 1983).
    Google Scholar 
    29.Riederer, M. & Schneider, G. Comparative study of the composition of waxes extracted from isolated leaf cuticules and from whole leaves of Citrus: evidence for selective extraction. Physiol. Plant 77, 373–384 (1989).CAS 
    Article 

    Google Scholar 
    30.Lendzian, K. J. & Kerstiens, G. Sorption and transport of gases and vapors in plant cuticles. Rev. Environ. Cont. Tox. 121, 65–128 (1991).CAS 

    Google Scholar 
    31.Kerstiens, G., Federholzner, R. & Lendzian, K. J. Dry deposition and cuticular uptake of pollutant gases. Agric. Ecosyst. Environ. 42, 239–253 (1992).CAS 
    Article 

    Google Scholar 
    32.Metzler, H. & Krause, B. Angewandte Statistik (Dt Verlag Wiss, 1983).
    Google Scholar 
    33.Baur, P. Lognormal distribution of water permeability and organic solute mobility in plant cuticles. Plant Cell Environ. 20, 167–177 (1997).ADS 
    CAS 
    Article 

    Google Scholar 
    34.Stamets, P. Growing Gourmet and Medicinal Mushrooms (Ten Speed Press, 1993).
    Google Scholar 
    35.Moser, M. Fungal growth and fructification under stress conditions. Ukrainian Botanical J. 50, 5–12 (1993).
    Google Scholar 
    36.Pinna, S., Gevry, M. F., Côté, M. & Sirois, L. Factors influencing fructification phenology of edible mushrooms in a boreal mixed forest of Eastern Canada. For. Ecol. Manag. 260(3), 294–301 (2010).Article 

    Google Scholar 
    37.Buller, A. H. R. Researches on Fungi. II. Further Investigations Upon the Production and Liberation of Spores in Hymenomyctes (Hafner Publishing Co, 1922).
    Google Scholar 
    38.Kües, U. Life history and developmental processes in the basidiomycete Coprinus cinereus. Microbiol. Mol. Biol. Rev. 64, 316–353 (2000).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    39.Money, N. More g’s than the space shuttle: ballistospore discharge. Mycologia 90, 547–558 (1998).Article 

    Google Scholar 
    40.Husher, J. et al. Evaporative cooling of mushrooms. Mycologia 91, 351–352 (1999).Article 

    Google Scholar 
    41.Dressaire, E., Yamada, L., Song, B. & Roper, M. Mushrooms use convectively created airflows to disperse their spores. Proc. Natl. Acad. Sci. U. S. A. 113, 2833–2838 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    42.De Groot, P. W., Schaap, P. J., Sonnenberg, A. S., Visser, J. & Van Griensven, L. J. The Agaricus bisporus hypAgene encodes a hydrophobin and specifically accumulates in peel tissue of mushroom caps during fruit body development. J. Mol. Biol. 257, 1008–1018 (1996).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    43.Wösten, H. A. B. & Wessels, J. G. H. The emergence of fruiting bodies in basidiomycetes. In Growth, Differentiation and Sexuality. The Mycota (A Comprehensive Treatise on Fungi as Experimental Systems for Basic and Applied Research), Vol. 1 (eds. Kües, U. & Fischer, R.) (Springer, 2006).44.Itoh, Y. H., Sugai, A., Uda, I. & Itoh, T. The evolution of lipids. Adv. Space Res. 28, 719–724 (2001).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    45.Segré, D., Ben-Eli, D., Deamer, D. W. & Lancet, D. The lipid world. Origins Life Evol. Biosphere 31, 119–145 (2001).ADS 
    Article 

    Google Scholar 
    46.Samson, R. A., Stalpers, J. A. & Verkerke, W. A simplified technique to prepare fungal specimens for scanning electronmicroscopy. Cytobios 24, 7–11 (1979).CAS 
    PubMed 
    PubMed Central 

    Google Scholar  More

  • in

    Revisiting traditional SSR based methodologies available for elephant genetic studies

    1.Whyte, I. Studying elephant movements, in studying elephants, in African Wildl. Found. Tech. Ser. 7. African Wildl. Found. (ed Kangwana, K.) 75–89 (1996).2.Rasmussen, L. E. L. & Krishnamurthy, V. How chemical signals integrate Asian elephant society: The known and the unknown. Zoo Biol. 19, 405–423 (2000).CAS 
    Article 

    Google Scholar 
    3.Nair, S., Balakrishnan, R., Seelamantula, C. S. & Sukumar, R. Vocalizations of wild Asian elephants (Elephas maximus ): structural classification and social context. J. Acoust. Soc. Am. 126, 2768–2778 (2009).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    4.Stoeger, A. S. & Manger, P. Vocal learning in elephants: neural bases and adaptive context. Curr. Opin. Neurobiol. 28, 101–107 (2014).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    5.Moss, C. J. & Poole, J. H. Relationships and social structure in African elephants. Primate Soc. Relationsh.: An Integr. Approach 315-325 (1983).
    Google Scholar 
    6.Foerder, P., Galloway, M., Barthel, T., Moore, D. E. & Reiss, D. Insightful problem solving in an asian elephant. PLoS ONE 6, e23251 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    7.Lee, P. C. Allomothering among African elephant. Animal Behaviour 35, 278-291 (1987).8.Byrne, R. W., Bates, L. & Moss, C. J. Comparative cognition & behavior reviews. Elephant Cogn. 4, 65–79 (2009).
    Google Scholar 
    9.Bates, L. A., Poole, J. H. & Byrne, R. W. Elephant cognition. Curr. Biol. 18, 544–546 (2008).Article 
    CAS 

    Google Scholar 
    10.Vance, E. A., Archie, E. A. & Moss, C. J. Social networks in African elephants. Comput. Math. Organ. Theory 15, 273–293 (2009).Article 

    Google Scholar 
    11.de Silva, S. & Wittemyer, G. A comparison of social organization in Asian elephants and African savannah elephants. Int. J. Primatol. 33, 1125–1141 (2012).Article 

    Google Scholar 
    12.Shoshani, J. Understanding proboscidean evolution: a formidable task. Trends Ecol. Evol. 13, 480–487 (1998).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    13.Rohland, N. et al. Proboscidean mitogenomics: chronology and mode of elephant evolution using mastodon as outgroup. PLoS Biol. 5, 1663–1671 (2007).CAS 
    Article 

    Google Scholar 
    14.de Flamingh, A. Genetic structure of the savannah elephant population (Loxodonta africana (Blumenbach 1797)) in the Kavango-Zambezi Transfrontier Conservation Area. ProQuest Diss. Theses 102 (2013).15.Grubb, P., Groves, C. P., Dudley, J. P. & Shoshani, J. Living African elephants belong to two species: Loxodonta africana (Blumenbach, 1797) and Loxodonta cyclotis (Matschie, 1900). Elephant 2, 1–4 (2000).Article 

    Google Scholar 
    16.Roca, A. L., Georgiadis, N., Pecon-Slattery, J. & O’Brien, S. J. Genetic evidence for two species of elephant in Africa. Science 293, 1473–1477 (2001).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    17.Roca, A. L. et al. Elephant natural history: a genomic perspective. Annu. Rev. Anim. Biosci. 3, 139–167 (2015).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    18.Wasser, S. K. et al. Assigning African elephant DNA to geographic region of origin: applications to the ivory trade. Proc. Natl. Acad. Sci. U. S. A. 101, 14847–14852 (2004).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    19.Ishida, Y. et al. Distinguishing forest and savanna African elephants using short nuclear DNA sequences. J. Hered. 102, 610–616 (2011).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    20.Comstock, K. E. et al. Patterns of molecular genetic variation among African elephant populations. Mol. Ecol. 11, 2489–2498 (2002).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    21.Palkopoulou, E. et al. A comprehensive genomic history of extinct and living elephants. Proc. Natl. Acad. Sci. U. S. A. 115, E2566–E2574 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    22.Shoshani, J. & Eisenberg, J. F. Elephas maximus. Mamm. Species 182, 1–8 (1982).Article 

    Google Scholar 
    23.Sukumar, R. The Living Elephants (Oxford University Press, 2003).
    Google Scholar 
    24.Sukumar, R. A brief review of the status, distribution and biology of wild Asian elephants Elephas maximus. Int. Zoo Yearb. 40, 1–8 (2006).Article 

    Google Scholar 
    25.Olivier, R. Distribution and status of the Asian elephant. Oryx 14(4), 379–424. https://doi.org/10.1017/S003060530001601X (1978).Article 

    Google Scholar 
    26.Santiapillai, C. The Asian elephant conservation: a global strategy. Gajah 18, 21–39 (1997).
    Google Scholar 
    27.Sukumar, R. Ecology of the Asian elephant in Southern India. i. movement and habitat utilization patterns. J. Trop. Ecol. 5, 1–18 (1989).Article 

    Google Scholar 
    28.Vidya, T. N. C., Fernando, P., Melnick, D. J. & Sukumar, R. Population genetic structure and conservation of Asian elephants (Elephas maximus) across India. Anim. Conserv. 8, 377–388 (2005).Article 

    Google Scholar 
    29.Fleischer, R. C., Perry, E. A., Muralidharan, K., Stevens, E. E. & Wemmer, C. M. Phylogeography of the Asian elephant (Elephas maximus) based on mitochondrial DNA. Evolution (N. Y.) 55, 1882–1892 (2001).CAS 

    Google Scholar 
    30.Fernando, P., Pfrender, M. E., Encalada, S. E. & Lande, R. Mitochondrial DNA variation, phylogeography and population structure of the Asian elephant. Heredity (Edinb). 84, 362–372 (2000).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    31.Fernando, P. Elephants in Sri Lanka: past, present, and future. Loris 22, 38–44 (2000).
    Google Scholar 
    32.Hendavitharana, W., Dissanayake, S. & de Silva, M. The survey of elephants in Sri Lanka. Gajah 12, 1–30 (1994).
    Google Scholar 
    33.Eggert, L. S., Rasner, C. A. & Woodruff, D. S. The evolution and phylogeography of the African elephant inferred from mitochondrial DNA sequence and nuclear microsatellite markers. Hungarian Q. 49, 1993–2006 (2008).
    Google Scholar 
    34.Ishida, Y., Georgiadis, N. J., Hondo, T. & Roca, A. L. Triangulating the provenance of African elephants using mitochondrial DNA. Evol. Appl. 6, 253–265 (2013).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    35.Liu, C. Z., Wang, L., Xia, X. J. & Jiang, J. Q. Characterization of the complete mitochondrial genome of cape elephant shrew, Elephantulus edwardii. Mitochondrial DNA Part B Resour. 3, 738–739 (2018).Article 

    Google Scholar 
    36.Fernando, P. et al. DNA analysis indicates that Asian elephants are native to Borneo and are therefore a high priority for conservation. PLoS Biol. 1, 110–115 (2003).CAS 
    Article 

    Google Scholar 
    37.Ahlering, M. A. et al. Genetic diversity, social structure, and conservation value of the elephants of the Nakai Plateau, Lao PDR, based on non-invasive sampling. Conserv. Genet. 12, 413–422 (2011).Article 

    Google Scholar 
    38.Goossens, B. et al. Habitat fragmentation and genetic diversity in natural populations of the Bornean elephant: implications for conservation. BIOC 196, 80–92 (2016).
    Google Scholar 
    39.Shoshani, J., Golenberg, E. M. & Yang, H. Elephantidae phylogeny: Morphological versus molecular results. Acta Theriol. (Warsz) 43, 89–122 (1998).Article 

    Google Scholar 
    40.Vidya, T. N. C. & Sukumar, R. Amplification success and feasibility of using microsatellite loci amplified from dung to population genetic studies of the Asian elephant (Elephas maximus). Curr. Sci. 88, 489–492 (2005).CAS 

    Google Scholar 
    41.Vidya, T. N. C., Varma, S., Dang, N. X., Van Thanh, T. & Sukumar, R. Minimum population size, genetic diversity, and social structure of the Asian elephant in Cat Tien National Park and its adjoining areas, Vietnam, based on molecular genetic analyses. Conserv. Genet. 8, 1471–1478 (2007).Article 

    Google Scholar 
    42.Suwattana, D., Jirasupphachok, J., Kanchanapangka, S. & Koykul, W. Tetranucleotide microsatellite markers for molecular testing in Thai domestic elephants (Elephas maximus indicus). Thai J. Vet. Med. 40, 405–409 (2010).
    Google Scholar 
    43.Eggert, L. S. et al. Using genetic profiles of African forest elephants to infer population structure, movements, and habitat use in a conservation and development landscape in Gabon. Conserv. Biol. 28, 107–118 (2014).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    44.Kinuthia, J. et al. The selection of a standard STR panel for DNA profiling of the African elephant (Loxodonta africana) in Kenya. Conserv. Genet. Resour. 7, 305–307 (2015).Article 

    Google Scholar 
    45.Hedges, S. Monitoring elephant populations and assessing threats. Universities Press (India) Pvt. Ltd., Hyderabad, India 259–292 (2012).46.Eggert, L. S., Ramakrishnan, U., Mundy, N. I. & Woodruff, D. S. Polymorphic microsatellite DNA markers in the African elephant (Loxondonta africana) and their use in the Asian elephant (Elephas maximus). Mol. Ecol. 9, 2222–2224 (2000).Article 

    Google Scholar 
    47.Nyakaana, S., Arctander, P. & Siegismund, H. R. Population structure of the African savannah elephant inferred from mitochondrial control region sequences and nuclear microsatellite loci. Heredity (Edinb). 89, 90–98 (2002).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    48.Kongrit, C. et al. Isolation and characterization of dinucleotide microsatellite loci in the Asian elephant (Elephas maximus). Mol. Ecol. Resour. 8, 175–177 (2007).Article 
    CAS 

    Google Scholar 
    49.Fernando, P., Vidya, T. N. C. & Melnick, D. J. Isolation and characterization of tri- and tetranucleotide microsatellite loci in the Asian elephant, Elephas maximus. Mol. Ecol. Resour. 8, 232–233 (2001).Article 

    Google Scholar 
    50.Archie, E. A., Moss, C. J. & Alberts, S. C. Characterization of tetranucleotide microsatellite loci in the African Savannah Elephant (Loxodonta africana africana). Mol. Ecol. Notes 3, 244–246 (2003).CAS 
    Article 

    Google Scholar 
    51.Lieckfeldt, D., Schmidt, A. & Pitra, C. Isolation and characterization of microsatellite loci in the great bustard, Otis tarda. Mol. Ecol. Notes 1, 133–134 (2001).CAS 
    Article 

    Google Scholar 
    52.Nyakaana, S., Okello, J. B. A., Muwanika, V. & Siegismund, H. R. Six new polymorphic microsatellite loci isolated and characterized from the African savannah elephant genome. Mol. Ecol. Notes 5, 223–225 (2005).CAS 
    Article 

    Google Scholar 
    53.Okello, J. B. A. et al. Population genetic structure of savannah elephants in Kenya: conservation and management implications. J. Hered. 99, 443–452 (2008).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    54.Nyakaana, S. & Arctander, P. Isolation and characterization of microsatellite loci in the African elephant, Loxodonta africana. Mol. Ecol. 10, 1436–1437 (1998).
    Google Scholar 
    55.Comstock, K. E., Wasser, S. K. & Ostrander, E. A. Polymorphic microsatellite DNA loci identified in the African elephant (Loxodonta africana). Mol. Ecol. 9, 1004–1006 (2000).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    56.Hartl, G. B., Hartl, K. F., Hemmer, W. & Nadlinger, K. Electrophoretic and chromosomal variation in captive Asian elephants (Elephas maximus). Zoo Biol. 14, 87–95 (1995).Article 

    Google Scholar 
    57.Bourgeois, S. et al. Single-nucleotide polymorphism discovery and panel characterization in the African forest elephant. Ecol. Evol. 8, 2207–2217 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    58.Sharma, R. et al. Two different high throughput sequencing approaches identify thousands of De Novo genomic markers for the genetically depleted Bornean elephant. PLoS ONE 7, e49533 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    59.Reddy, P. C. et al. Comparative sequence analyses of genome and transcriptome reveal novel transcripts and variants in the Asian elephant Elephas maximus. J. Biosci. 40, 891–907 (2015).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    60.Mondol, S. et al. New evidence for hybrid zones of forest and savanna elephants in Central and West Africa. Mol. Ecol. 24, 6134–6147 (2015).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    61.Hou, Z. C. et al. Elephant transcriptome provides insights into the evolution of eutherian placentation. Genome Biol. Evol. 4, 713–725 (2012).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    62.Tollis, M. et al. Elephant Genomes Reveal Insights into Differences in Disease Defense Mechanisms between Species. bioRxiv 2020.05.29.124396 (2020).63.Rohland, N. et al. Genomic DNA sequences from mastodon and woolly mammoth reveal deep speciation of forest and savanna elephants. PLoS Biol. 8, 16–19 (2010).Article 
    CAS 

    Google Scholar 
    64.Lynch, V. J. et al. Elephantid genomes reveal the molecular bases of woolly mammoth adaptations to the Arctic. Cell Rep. 12, 217–228 (2015).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    65.Yang, H., Golenberg, E. M. & Shoshani, J. Phylogenetic resolution within the elephantidae using fossil DNA sequence from the American mastodon (Mammut americanum) as an outgroup. Proc. Natl. Acad. Sci. U. S. A. 93, 1190–1194 (1996).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    66.Orlando, L., Hänni, C. & Douady, C. J. Mammoth and elephant phylogenetic relationships: Mammut americanum, the missing outgroup. Evol. Bioinforma. 3, 45–51 (2007).CAS 
    Article 

    Google Scholar 
    67.Eggert, L. S., Eggert, J. A. & Woodruff, D. S. Estimating population sizes for elusive animals: the forest elephants of Kakum National Park, Ghana. Mol. Ecol. 12, 1389–1402 (2003).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    68.Vidya, T. N. C. Evolutionary history and population genetic structure of Asian elephants in India. Indian J. Hist. Sci. 51, 391–405 (2016).
    Google Scholar 
    69.Schuttler, S. G., Whittaker, A., Jeffery, K. J. & Eggert, L. S. African forest elephant social networks: fission-fusion dynamics, but fewer associations. Endanger. Species Res. 25, 165–173 (2014).Article 

    Google Scholar 
    70.Ahlering, M. A. et al. Identifying source populations and genetic structure for savannah elephants in human-dominated landscapes and protected areas in the Kenya-Tanzania borderlands. PLoS ONE 7, e52288 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    71.Vidya, T. N. C., Fernando, P., Melnick, D. J. & Sukumar, R. Population differentiation within and among Asian elephant (Elephas maximus) populations in southern India. Heredity (Edinb). 94, 71–80 (2005).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    72.Sukumar, R., Ramakrishnan, U. & Santosh, J. A. Impact of poaching on an Asian elephant population in Periyar, southern India: a model of demography and tusk harvest. Anim. Conserv. 1, 281–291 (1998).Article 

    Google Scholar 
    73.Mondol, S., Mailand, C. R. & Wasser, S. K. Male biased sex ratio of poached elephants is negatively related to poaching intensity over time. Conserv. Genet. 15, 1259–1263 (2014).Article 

    Google Scholar 
    74.Breuer, T., Maisels, F. & Fishlock, V. The consequences of poaching and anthropogenic change for forest elephants. Conserv. Biol. 30, 1019–1026 (2016).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    75.Mailand, C. & Wasser, S. K. Isolation of DNA from small amounts of elephant ivory. Nat. Protoc. 2, 2228–2232 (2007).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    76.Lee, E. et al. The identification of elephant ivory evidences of illegal trade with mitochondrial cytochrome b gene and hypervariable D-loop region. J. Forensic Leg. Med. 20, 174–178 (2015).Article 

    Google Scholar 
    77.Chakraborty, S., Boominathan, D., Desai, A. A. & Vidya, T. N. C. Using genetic analysis to estimate population size, sex ratio, and social organization in an Asian elephant population in conflict with humans in Alur, southern India. Conserv. Genet. 15, 897–907 (2014).Article 

    Google Scholar 
    78.Fernando, P. & Pastorini, J. Range-wide status of Asian elephants. Gajah 35, 15–20 (2011).
    Google Scholar 
    79.Ishida, Y., Gugala, N. A., Georgiadis, N. J. & Roca, A. L. Evolutionary and demographic processes shaping geographic patterns of genetic diversity in a keystone species, the African forest elephant (Loxodonta cyclotis). Ecol. Evol. 8, 4919–4931 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    80.Kongrit, C. Genetic tools for the conservation of wild Asian elephants. Int. J. Biol. 9, 1 (2017).Article 

    Google Scholar 
    81.McComb, K., Shannon, G., Sayialel, K. N. & Moss, C. Elephants can determine ethnicity, gender, and age from acoustic cues in human voices. Proc. Natl. Acad. Sci. U. S. A. 111, 5433–5438 (2014).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    82.Prithiviraj, F. & Melnick, D. J. Molecular sexing eutherina mammals. Mol. Ecol. Notes 1, 350–353 (2001).Article 

    Google Scholar 
    83.Vandebona, H. et al. DNA fingerprints of the Asian elephant in Sri Lanka, Elephas maximus maximus, using multilocus probe 33.15 (Jeffreys). J. Natl. Sci. Found. Sri Lanka 32, 83–96 (2004).CAS 
    Article 

    Google Scholar 
    84.Gugala, N. A., Ishida, Y., Georgiadis, N. J. & Roca, A. L. Development and characterization of microsatellite markers in the African forest elephant (Loxodonta cyclotis). BMC Res. Notes 9, 4–9 (2016).Article 
    CAS 

    Google Scholar 
    85.Zhang, L. et al. Asian elephants in China: estimating population size and evaluating habitat suitability. PLoS ONE 10, 1–13 (2015).
    Google Scholar 
    86.Vartia, S. et al. A novel method of microsatellite genotyping-by-sequencing using individual combinatorial barcoding. R. Soc. Open Sci. 3, 150565 (2016).ADS 
    MathSciNet 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    87.Tighe, A. J. et al. Testing PCR amplification from elephant dung using silica-dried swabs. Pachyderm 59, 56–65 (2018).
    Google Scholar 
    88.Bourgeois, S. et al. Improving cost-efficiency of faecal genotyping: new tools for elephant species. PLoS ONE 14, e0210811 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    89.Hedges, S., Johnson, A., Ahlering, M., Tyson, M. & Eggert, L. S. Accuracy, precision, and cost-effectiveness of conventional dung density and fecal DNA based survey methods to estimate Asian elephant (Elephas maximus) population size and structure. Biol. Conserv. 159, 101–108 (2013).Article 

    Google Scholar 
    90.Moßbrucker, A. M. et al. Non-invasive genotyping of Sumatran elephants : implications for conservation The Sumatran elephant (Elephas maximus sumatranus) is one of three currently recognized subspecies. Trop. Conserv. Sci. 8, 745–759 (2015).Article 

    Google Scholar 
    91.Ishida, Y. et al. Short amplicon microsatellite markers for low quality elephant DNA. Conserv. Genet. Resour. 4, 491–494 (2012).Article 

    Google Scholar 
    92.Thitaram, C. et al. Evaluation and selection of microsatellite markers for an identification and parentage test of Asian elephants (Elephas maximus). Conserv. Genet. 9, 921–925 (2008).CAS 
    Article 

    Google Scholar 
    93.Lorenz, T. C. Polymerase chain reaction: basic protocol plus troubleshooting and optimization strategies. J. Vis. Exp. 2, 1–15. https://doi.org/10.3791/3998 (2012).CAS 
    Article 

    Google Scholar 
    94.Litt, M. & Luty, J. A. Hypervariable amplification. Am. J. Hum. Genet. 44, 397–401 (1989).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    95.Park, Y. J., Lee, J. K. & Kim, N. S. Simple sequence repeat polymorphisms (SSRPs) for evaluation of molecular diversity and germplasm classification of minor crops. Molecules 14, 4546–4569 (2009).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    96.Vieira, M. L. C., Santini, L., Diniz, A. L. & Munhoz, C. D. F. Microsatellite markers: what they mean and why they are so useful. Genet. Mol. Biol. 39, 312–328 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    97.Stafne, E. T., Clark, J. R., Weber, C. A., Graham, J. & Lewers, K. S. Simple sequence repeat (SSR) markers for genetic mapping of raspberry and blackberry. J. Am. Soc. Hortic. Sci. 130, 722–728 (2005).CAS 
    Article 

    Google Scholar 
    98.Tommasini, L. et al. The development of multiplex simple sequence repeat (SSR) markers to complement distinctness, uniformity and stability testing of rape (Brassica napus L.) varieties. Theor. Appl. Genet. 106, 1091–1101 (2003).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    99.Norrgard, K. Forensics, DNA Fingerprinting, and CODIS. Nat. Educ. 1, 35 (2008).
    Google Scholar 
    100.Maroju, P. A. et al. Schrodinger’s scat: A critical review of the currently available tiger (Panthera Tigris) and leopard (Panthera pardus) specific primers in India, and a novel leopard specific primer. BMC Genet. 17, 1–6 (2016).Article 

    Google Scholar 
    101.Waits, L. P. & Pearkau, D. Noninvasive genetic sampling tools for wildlife biologists: a review of applications and recommendations for accurate data collection. J. Wildl. Manag. 69, 1419–1433 (2005).Article 

    Google Scholar 
    102.Baird, N. A. et al. Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS ONE 3, 1–7 (2008).Article 
    CAS 

    Google Scholar 
    103.Miller, M. R., Dunham, J. P., Amores, A., Cresko, W. A. & Johnson, E. A. Rapid and cost-effective polymorphism identification and genotyping using restriction site associated DNA (RAD) markers. Genome Res. 17, 240–248 (2007).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    104.Delord, C. et al. A cost-and-time effective procedure to develop SNP markers for multiple species: a support for community genetics. Methods Ecol. Evol. 9, 1959–1974 (2018).Article 

    Google Scholar 
    105.Magwanga, R. O. et al. GBS mapping and analysis of genes conserved between Gossypium tomentosum and Gossypium hirsutum cotton cultivars that respond to drought stress at the seedling stage of the BC2F2generation. Int. J. Mol. Sci. 19, 1614 (2018).PubMed Central 
    Article 
    CAS 

    Google Scholar 
    106.Elshire, R. J. et al. A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6, 1–10 (2011).Article 
    CAS 

    Google Scholar 
    107.Chandrasekara, C. H. W. M. R. B., Wijesundera, W. S. S., Perera, H. N., Chong, S. S. & Rajan-Babu, I. S. Cascade screening for fragile X syndrome/CGG repeat expansions in children attending special education in Sri Lanka. PLoS ONE 10, 1–10 (2015).
    Google Scholar 
    108.Felsenstein, J. 2002. {PHYLIP}(Phylogen. I. P. ver. 3. 6a3.—P. by the author. PHYLIP(Phylogeny Inference Package) ver. 3.6a3. (2002).109.Nei, M. & Li, W. H. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc. Natl. Acad. Sci. U. S. A. 76, 5269–5273 (1979).ADS 
    CAS 
    PubMed 
    PubMed Central 
    MATH 
    Article 

    Google Scholar 
    110.Rambaut, A. FigTree ver.1. 3.1: tree figure drawing tool. http://tree.bio.ed.ac.uk/software/figtree. (2009). More

  • in

    Keeping an eye on the use of eye-lens weight as a universal indicator of age for European wild rabbits

    1.Stearns, S. C. The Evolution of Life Histories (Oxford University Press, 1992).
    Google Scholar 
    2.Caughley, G. & Sinclair, A. R. E. Wildlife Ecology and Management (Blackwell Science, 1994).
    Google Scholar 
    3.Servanty, S. et al. Influence of harvesting pressure on demographic tactics: Implications for wildlife management. J. Appl. Ecol. 48(4), 835–843 (2011).Article 

    Google Scholar 
    4.Marboutin, E., Bray, Y., Péroux, R., Mauvy, B. & Lartiges, A. Population dynamics in European hare: Breeding parameters and sustainable harvest rates. J. Appl. Ecol. 40(3), 580–591 (2003).Article 

    Google Scholar 
    5.Stoneberg, R. P. & Jonkel, C. L. Age determination of black bears by cementum layers. J. Wildlife Manage. 30(2), 411–414 (1966).Article 

    Google Scholar 
    6.Roth, V. L. & Shoshani, J. Dental identification and age determination in Elephas maximus. J. Zool. 214, 567–588 (1988).Article 

    Google Scholar 
    7.Dutta, S. & Sengupta, P. Men and mice: Relating their ages. Life Sci. 152, 244–248 (2016).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    8.Dimmick, R. W. & Pelton, M. R. Criteria of sex and age. In Research and Management Techniques for Wildlife and Habitats 5th edn, (ed. Bookhout, T.
    A.) 169–214 (The Wildlife Society, Bethesda, MA, US, 1994).
    Google Scholar 
    9.Morris, P. A review of mammalian age determination methods. Mamm. Rev. 2, 69–103 (1972).Article 

    Google Scholar 
    10.Augusteyn, R. C. On the relationship between rabbit age and lens dry weight: Improved determination of the age of rabbits in the wild. Mol. Vis. 13, 2030–2034 (2007).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    11.Augusteyn, R. C. Growth of the lens: In vitro observations. Clin. Exp. Optom. 91(3), 226–239 (2008).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    12.Augusteyn, R. C. Growth of the eye lens: I. Weight accumulation in multiple species. Mol. Vis. 20, 410–426 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    13.Lord, D. R. The lens as an indicator of age in cottontail rabbits. J. Wildl. Manage. 23, 358–360 (1959).Article 

    Google Scholar 
    14.Forsyth, D. M., Garel, M. & McLeod, S. R. Estimating age and age class of harvested hog deer from eye lens mass using frequentist and Bayesian methods. Wildlife biol. 22(4), 137–143 (2016).Article 

    Google Scholar 
    15.Dudzinski, M. L. & Mykytowycz, R. The eye lens as an indicator of age in the wild rabbit in Australia. CSIRO Wildl. Res. 6, 156–159 (1961).Article 

    Google Scholar 
    16.Myers, K. & Gilbert, N. Determination of age of wild rabbits in Australia. J. Wildl. Manage. 32, 841–849 (1968).Article 

    Google Scholar 
    17.Wheeler, S. H. & King, D. R. The use of eye-lens weights for aging wild rabbits, Oryctolagus cuniculus (L.) in Australia. Aust. Wildl. Res. 7, 79–84 (1980).Article 

    Google Scholar 
    18.Tablado, Z., Revilla, E. & Palomares, F. Breeding like rabbits: Global patterns of variability and determinants of European wild rabbit reproduction. Ecography 32, 310–320. https://doi.org/10.1111/j.1600-0587.2008.05532.x (2009).Article 

    Google Scholar 
    19.Ferreira, C. et al. Biometrical analysis reveals major differences between the two subspecies of the European rabbit. Biol. J. Linn. Soc. 116, 106–116 (2015).Article 

    Google Scholar 
    20.Branco, M., Monnerot, M., Ferrand, N. & Templeton, A. R. Postglacial dispersal of the European rabbit (Oryctolagus cuniculus) on the Iberian Peninsula reconstructed from nested clade and mismatch analyses of mitochondrial DNA genetic variation. Evolution 56, 792–803. https://doi.org/10.1111/j.0014-3820.2002.tb01390.x (2002).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    21.Gómez, A. & Lunt, D. H. Refugia within refugia: Patterns of phylogeographic concordance in the Iberian Peninsula. In Phylogeography in Southern European Refugia (eds Weiss, S. & Ferrand, N.) 155–188 (Springer, 2006).
    Google Scholar 
    22.Geraldes, A. et al. Reduced introgression of the Y chromosome between subspecies of the European rabbit (Oryctolagus cuniculus) in the Iberian Peninsula. Mol. Ecol. 17, 4489–4499 (2008).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    23.Carneiro, M., Ferrand, N. & Nachman, M. W. Recombination and speciation: Loci near centromeres are more differentiated than loci near telomeres between subspecies of the European rabbit (Oryctolagus cuniculus). Genetics 181, 593–606 (2009).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    24.Rafati, N. et al. A genomic map of clinal variation across the European rabbit hybrid zone. Mol. Ecol. 27, 1457–1478. https://doi.org/10.1111/mec.14494 (2018).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    25.Vaquerizas, P. H. et al. The paradox of endangered European rabbits regarded as pests in the Iberian Peninsula: Subspecies differences in trends matter. Endang. Species Res. 43, 99–102 (2020).Article 

    Google Scholar 
    26.Arques, J. & Peiró, V. Estructura de Sexos y Edades de una población de Conejos (Oryctolagus cuniculus) del sudeste de España. Mediterránea. Serie de Estudios Biológicos 18, 1–33 (2005).
    Google Scholar 
    27.Trout, R. C. & Smith, G. C. The reproductive productivity of the wild rabbit (Oryctolagus cuniculus) in southern England on sites with different soils. J. Zool. 237(3), 411–422 (1995).Article 

    Google Scholar 
    28.Boussès, P., Arthur, C. & Chapuis, J. L. Rôle du facteur trophique sur la biologie des populations de lapins (Oryctolagus cuniculus L.) des Iles Kerguelen. Revue d’écologie 43, 329–343 (1988).
    Google Scholar 
    29.Bonino, N. & Donadio, E. Body parameters and sexual dimorphism in the European wild rabbit (Oryctolagus cuniculus) introduced in Argentina. Mastozool. Neotrop. 17(1), 123–127 (2010).
    Google Scholar 
    30.Carneiro, M. et al. Rabbit genome analysis reveals a polygenic basic for phenotypic change during domestication. Science 345(6200), 1074–1079 (2014).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    31.Myers, K. The rabbit in Australia. In Dynamics of Numbers in Populations (eds den Boer, P. J. & Gradwell, G. R.) 478–506 (Proceedings of the NATO Advanced Study Institute Oosterbeek, 1970).
    Google Scholar 
    32.Delibes-Mateos, M., Villafuerte, R., Cooke, B. & Alves, P. C. Oryctolagus cuniculus (Linnaeus, 1758). In Lagomorphs: Pikas, Rabbits and Hares of the World (eds Smith, A. T. et al.) 99–104 (John Hopkins University Press, 2018).
    Google Scholar 
    33.Carneiro, M. et al. The genomic architecture of population divergence between subspecies of the European rabbit. PLoS. Genet. 10(8), e1003519. https://doi.org/10.1371/journal.pgen.1003519 (2014).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    34.Bonino, N. & Soriguer, R. Genetic lineages of feral populations of the Oryctolagus cuniculus (Leporidae, Lagomorpha) in Argentina. Mammalia 72, 355–357 (2008).Article 

    Google Scholar 
    35.Branco, M. & Ferrand, N. Biochemical and population genetics of the rabbit, Oryctolagus cuniculus, carbonic anhydrases I and II, from the Iberian Peninsula and France. Biochem. Genet. 41, 391–404. https://doi.org/10.1023/B:BIGI.0000007774.39262.8e (2003).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    36.Geraldes, A., Ferrand, N. & Nachman, M. W. Contrasting patterns of introgression at X-linked loci across the hybrid zone between subspecies of the European rabbit (Oryctolagus cuniculus). Genetics 173, 919–933 (2006).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    37.Lo Valvo, M., Scala, A. & Scalisi, M. Biometric characterization and taxonomic considerations of European rabbit Oryctolagus cuniculus (Linnaeus 1758) in Sicily (Italy). World Rabbit Sci. 22(3), 207–214. https://doi.org/10.4995/wrs.2014.1467 (2014).Article 

    Google Scholar 
    38.Miller, G. S. Catalogue of the Mammals of Western Europe in the Collection of the British Museum (Trustees of the British Museum, 1912).
    Google Scholar 
    39.Sharples, C. M., Fa, J. E. & Bell, D. J. Geographical variation in size in the European rabbit Oryctolagus cuniculus (Lagomorpha: Leporidae) in western Europe and North Africa. Zool. J. Linn. Soc-Lond. 117, 141–158. https://doi.org/10.1111/j.1096-3642.1996.tb02153.x (1996).Article 

    Google Scholar 
    40.Carro, F., Ortega, M. & Soriguer, R. C. Is restocking a useful tool for increasing rabbit densities?. Global Ecol. Conserv. 17, e00560. https://doi.org/10.1016/j.gecco.2019.e00560 (2019).Article 

    Google Scholar 
    41.Angulo, E. & Villafuerte, R. Modelling hunting strategies for the conservation of wild rabbit populations. Biol. Conserv. 115, 291–301 (2003).Article 

    Google Scholar 
    42.Delibes-Mateos, M., Delibes, M., Ferreras, P. & Villafuerte, R. Key role of European rabbits in the conservation of the Western Mediterranean Basin Hotspot. Conserv. Biol. 22, 1106–1117 (2008).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    43.Garrido, J. L., Ferreres, J. & Gortázar, C. Las especies cinegéticas españolas en el siglo XXI. (eds. Garrido, J. L., Ferreres, J. & Gortázar, C.)
    (Independently published, Ciudad Real, Spain, 2019).
    Google Scholar 
    44.Ríos-Saldaña, C. et al. Control of the European rabbit in central Spain. Eur. J. Wildlife Res. 59, 573–580. https://doi.org/10.1007/s10344-013-0707-x (2013).Article 

    Google Scholar 
    45.Lees, A. C. & Bell, D. J. A conservation paradox for the 21st century: The European wild rabbit Oryctolagus cuniculus, an invasive alien and an endangered native species. Mammal Rev. 38, 304–320 (2008).Article 

    Google Scholar 
    46.Cooke, B. D. Rabbits: Manageable environmental pests or participants in new Australian ecosystems?. Wildlife Res. 39, 279–289 (2013).ADS 
    Article 

    Google Scholar 
    47.Calvete, C., Angulo, E. & Estrada, R. Conservation of European wild rabbit populations when hunting is age and sex selective. Biol. Conserv. 121(4), 623–634 (2005).Article 

    Google Scholar 
    48.Delibes-Mateos, M., Ramírez, E., Ferreras, P. & Villafuerte, R. Translocations as a risk for the conservation of European wild rabbit Oryctolagus cuniculus lineages. Oryx 42(2), 259–264 (2008).Article 

    Google Scholar 
    49.Andersen, J. & Jensen, B. Studies on the European hare. XXVIII. The weight of the eye lens in the European hares of known age. Acta Theriol. 17, 87–92 (1972).Article 

    Google Scholar 
    50.Suchentrunck, F., Willing, R. & Hartl, G. B. On eye lens weights and other age criteria of the Brown hare (Lepus europaeus Pallas, 1778). Z. Säugetierkd. 56, 365–374 (1991).
    Google Scholar 
    51.Villafuerte, R. et al. Large-scale assessment of myxomatosis prevalence in European wild rabbits (Oryctolagus cuniculus) 60 years after first outbreak in Spain. Res. Vet. Sci. 114, 281–286 (2017).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    52.Rouco, C., Villafuerte, R., Castro, F. & Ferreras, P. Effect of artificial warren size on a restocked European wild rabbit population. Anim. Conserv. 14, 117–123 (2011).Article 

    Google Scholar 
    53.Southern, N. The ecology and population dynamics of the wild rabbit (Oryctolagus cuniculus). Ann. Appl. Biol. 27, 509–514 (1940).Article 

    Google Scholar 
    54.Dunnet, G. M. Growth rate of young rabbits, Oryctolagus cuniculus (L.). CSIRO Wildl. Res. 1, 66–67 (1956).Article 

    Google Scholar 
    55.Ferreira, A. & Ferreira, A. J. Post-weaning growth of endemic Iberian wild rabbit subspecies, Oryctolagus cuniculus algirus, kept in a semi-extensive enclosure: Implications for management and conservation. World Rabbit Sci. 22, 129–136. https://doi.org/10.4995/wrs.2014.1673 (2014).Article 

    Google Scholar 
    56.R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ (Vienna,
    Austria, 2020).
    Google Scholar 
    57.du Sert, N. P. et al. Reporting animal research: Explanation and elaboration for the ARRIVE guidelines 2.0. PLoS Biol. 18(7), e3000411. https://doi.org/10.1371/journal.pbio.3000411 (2020).MathSciNet 
    CAS 
    Article 

    Google Scholar 
    58.Burnham, K. P. & Anderson, D. R. Monte Carlo insights and extended examples. In Model Selection and Multimodel Inference, (eds. Burnham K. P. &
    Anderson D. R.) https://doi.org/10.1007/978-0-387-22456-5_5). (Springer, New York, NY, US, 2002).59.Pastore, M. Overlapping: A R package for estimating overlapping in empirical distributions. J. Open Source Softw. 32, 1023 (2018).ADS 
    Article 

    Google Scholar 
    60.Pastore, M. & Calcagnì, A. Measuring distribution similarities between samples: A distribution-free overlapping Index. Front. Psychol. 10, 1089 https://doi.org/10.3389/fpsyg.2019.01089 (2019).Article 

    Google Scholar 
    61.Williams, C. & Moore, R. Phenotypic adaptation and natural selection in the wild rabbit, Oryctolagus cuniculus, Australia. J. Anim. Ecol. 58(2), 495–507. https://doi.org/10.2307/4844 (1989).Article 

    Google Scholar  More

  • in

    New lineages of photobionts in Bolivian lichens expand our knowledge on habitat preferences and distribution of Asterochloris algae

    1.Fernández-Brime, S., Muggia, L., Maier, S., Grube, M. & Wedin, M. Bacterial communities in an optional lichen symbiosis are determined by substrate, not algal photobionts. FEMS Microbiol. Ecol. 95, fiz012 (2019).PubMed 
    Article 
    CAS 

    Google Scholar 
    2.Grube, M. et al. Exploring functional contexts of symbiotic sustain within lichen-associated bacteria by comparative omics. ISME J. 9, 412–424 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    3.Spribille, T. et al. Basidiomycete yeasts in the cortex of ascomycete macrolichens. Science 353, 488–492 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    4.Peksa, O. & Škaloud, P. Do photobionts influence the ecology of lichens? A case study of environmental preferences in symbiotic green alga Asterochloris (Trebouxiophyceae). Mol. Ecol. 20, 3936–3948 (2011).PubMed 
    Article 

    Google Scholar 
    5.Řídká, T., Peksa, O., Rai, H., Upreti, D. K. & Škaloud, P. Photobiont diversity in Indian Cladonialichens, with special emphasis on the geographical patterns. In Terricolous Lichens in India, Volume 1: Diversity Patterns and Distribution Ecology (eds Rai, H. & Upreti, D. K.) 53–71 (Springer, New York, 2014).
    Google Scholar 
    6.Rolshausen, G. et al. Expanding the mutualistic niche: Parallel symbiont turnover along climatic gradients. Proc. R. Soc. B 287, 1924 (2020).Article 

    Google Scholar 
    7.Kosecka, M. et al. Trentepohlialean algae (Trentepohliales, Ulvophyceae) show preference to selected mycobiont lineages in lichen symbioses. J. Phycol. 56, 979–993 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    8.Muggia, L., Pérez-Ortega, S., Kopun, T., Zellnig, G. & Grube, M. Photobiont selectivity leads to ecological tolerance and evolutionary divergence in a polymorphic complex of lichenized fungi. Ann. Bot. 114, 463–475 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    9.Vančurová, L., Muggia, L., Peksa, O., Řídká, T. & Škaloud, P. The complexity of symbiotic interactions influences the ecological amplitude of the host: A case study in Stereocaulon (lichenized Ascomycota). Mol. Ecol. 27, 3016–3033 (2018).PubMed 
    Article 
    CAS 

    Google Scholar 
    10.Beck, A., Kasalicky, T. & Rambold, G. Myco-photobiontal selection in a Mediterranean cryptogam community with Fulgensia fulgida. New Phytol. 153, 317–326 (2002).Article 

    Google Scholar 
    11.Nelsen, M. P. & Gargas, A. Actin type intron sequences increase phylogenetic resolution: An example from Asterochloris (Chlorophyta: Trebouxiophyceae). Lichenologist 38, 435–440 (2006).Article 

    Google Scholar 
    12.Nelsen, M. P. & Gargas, A. Dissociation and horizontal transmission of co-dispersed lichen symbionts in the genus Lepraria (Lecanorales: Stereocaulaceae). New Phytol. 177, 264–275 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    13.Škaloud, P. & Peksa, O. Evolutionary inferences based on ITS rDNA and actin sequences reveal extensive diversity of the common lichen alga Asterochloris. Mol. Phylogenet. Evol. 54, 36–46 (2010).PubMed 
    Article 

    Google Scholar 
    14.Škaloud, P., Steinová, J., Řídká, T., Vančurová, L. & Peksa, O. Assembling the challenging puzzle of algal biodiversity: Species delimitation within the genus Asterochloris (Trebouxiophyceae, Chlorophyta). J. Phycol. 51, 507–527 (2015).PubMed 
    Article 
    CAS 

    Google Scholar 
    15.Steinová, J., Škaloud, P., Yahr, R., Bestová, H. & Muggia, L. Reproductive and dispersal strategies shape the diversity of mycobiont-photobiont association in Cladonia lichens. Mol. Phylogenet. Evol. 134, 226–237 (2019).PubMed 
    Article 

    Google Scholar 
    16.Vančurová, L., Peksa, O., Němcová, Y. & Škaloud, P. Vulcanochloris (Trebouxiales, Trebouxiophyceae), a new genus of lichen photobiont from La Palma, Canary Islands, Spain. Phytotaxa 219, 118–132 (2015).Article 

    Google Scholar 
    17.Vančurová, L. et al. Symbiosis between river and dry lands: Phycobiont dynamics on river gravel bars. Algal Res. 51, 102062. https://doi.org/10.1016/j.algal.2020.102062 (2020).Article 

    Google Scholar 
    18.Yahr, R., Vilgalys, R. & Depriest, P. T. Strong fungal specificity and selectivity for algal symbionts in Florida scrub Cladonia lichens. Mol. Ecol. 13, 3367–3378 (2004).CAS 
    PubMed 
    Article 

    Google Scholar 
    19.Tschermak-Woess, E. Asterochloris phycobiontica gen. et spec. nov., der Phycobiont der Flechte Varicellaria carneonivea. Plant Syst. Evol. 135, 279–294 (1980).Article 

    Google Scholar 
    20.Moya, P. et al. Molecular phylogeny and ultrastructure of the lichen microalga Asterochloris mediterranea sp. Nov. from Mediterranean and Canary Islands ecosystems. Int. J. Syst. Evol. Microbiol. 65(6), 1838–1854 (2015).PubMed 
    Article 
    CAS 

    Google Scholar 
    21.Kim, J. I. et al. Asterochloris sejongensis sp. nov. (Trebouxiophyceae, Chlorophyta) from King George Island, Antarctica. Phytotaxa 295, 60–70 (2017).Article 

    Google Scholar 
    22.Kim, J. I. et al. Taxonomic study of three new Antarctic Asterochloris(Trebouxio-phyceae) based on morphological and molecular data. Korean Soc. Phycol. 35(1), 17–32 (2020).CAS 

    Google Scholar 
    23.Pino-Bodas, R. & Stenroos, S. Global biodiversity patterns of the photobionts associated with the genus Cladonia (Lecanorales, Ascomycota). Microb. Ecol. https://doi.org/10.1007/s00248-020-01633-3 (2020).Article 
    PubMed 

    Google Scholar 
    24.Fernandez-Mendoza, F. et al. Population structure of mycobionts and photobionts of the widespread lichen Cetraria aculeata. Mol. Ecol. 20, 1208–1232 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    25.Helms, G. Taxonomy and symbiosis in associations of Physciaceae and Trebouxia. Göttingen, Doctoral thesis. Germany: Georg-August Universität Göttingen (2003).26.Kroken, S. & Taylor, J. W. Phylogenetic species, reproductive mode, and specificity of the green alga Trebouxia forming lichens with the fungal genus Letharia. Bryologist 103, 645–660 (2000).CAS 
    Article 

    Google Scholar 
    27.Leavitt, S. D. et al. Fungal specificity and selectivity for algae play a major role in determining lichen partnerships across diverse ecogeographic regions in the lichen- forming family Parmeliaceae (Ascomycota). Mol. Ecol. 24, 3779–3797 (2015).PubMed 
    Article 

    Google Scholar 
    28.Magain, N., Miadlikowska, J., Goffinet, B., Sérusiaux, E. & Lutzoni, F. Macroevolution of Specificity in Cyanolichens of the Genus Peltigera Section Polydactylon (Lecanoromycetes, Ascomycota). Syst. Biol. 66, 74–99 (2016).
    Google Scholar 
    29.Mark, K. et al. Contrasting cooccurrence patterns of photobiont and cystobasidiomycete yeast associated with common epiphytic lichen species. New Phytol. 227, 1362–1375 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    30.O’Brien, H. E., Miadlikowska, J. & Lutzoni, F. Assessing population structure and host specialization in lichenized cyanobacteria. New Phytol. 198, 557–566 (2013).PubMed 
    Article 

    Google Scholar 
    31.Piercey-Normore, M. D. & DePriest, P. T. Algal switching among lichen symbionts. Am. J. Bot. 88, 1490–1498 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    32.Yahr, R., Vilgalys, R. & DePriest, P. T. Geographic variation in algal partners of Cladonia subtenuis (Cladoniaceae) highlights the dynamic nature of a lichen symbiosis. New Phytol. 171, 847–860 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    33.Muggia, L. et al. The symbiotic playground of lichen thalli—A highly flexible photobiont association in rock inhabiting lichens. FEMS Microbiol. Ecol. 85, 313–323 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    34.Sadowska-Deś, A. D. et al. Integrating coalescent and phylogenetic approaches to delimit species in the lichen photobiont Trebouxia. Mol. Phylogenet. Evol. 76, 202–210 (2014).PubMed 
    Article 

    Google Scholar 
    35.Wirtz, N. et al. Lichen fungi have low cyanobiont selectivity in maritime Antarctica. New Phytol. 160, 177–183 (2003).Article 

    Google Scholar 
    36.Ertz, D., Guzow-Krzemińska, B., Thor, G., Łubek, A. & Kukwa, M. Photobiont switching causes changes in the reproduction strategy and phenotypic dimorphism in the Arthoniomycetes. Sci Rep. 8, 4952 (2018).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    37.Marshall, W. A. & Chalmers, M. O. Airborne dispersal of Antarctic terrestrial algae and cyanobacteria. Ecography 20, 585–594 (1997).Article 

    Google Scholar 
    38.Printzen, C., Domaschke, S., Fernandez-Mendoza, F. & Perez-Ortega, S. Biogeography and ecology of Cetraria aculeata, a widely distributed lichen with a bipolar distribution. MycoKeys 6, 33–53 (2013).Article 

    Google Scholar 
    39.Pardo-De la Hoz, C. J. et al. Contrasting symbiotic patterns in two closely related lineages of trimembered lichens of the genus Peltigera. Front. Microbiol. 9, 2770–2770 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    40.Singh, G. et al. Fungal–algal association patterns in lichen symbiosis linked to macroclimate. New Phytol. 214, 317–329 (2017).PubMed 
    Article 

    Google Scholar 
    41.Cordeiro, L. M. C. et al. Molecular studies of photobionts of selected lichens from the coastal vegetation of Brazil. FEMS Microbiol. Ecol. 54, 381–390 (2005).CAS 
    PubMed 
    Article 

    Google Scholar 
    42.Pullaiah, T. (ed.) (2019) Biodiversity in Bolivia in: Global Biodiversity Volume 4: Selected Countries in the Americas and Australia, Chapter 1. 1–574 (Apple Academic Press, 2001).43.Ibisch, P. L. & Mérida, G. Biodiversity: the richness of Bolivia. State of knowledge and conservation. 1–638 (Ministry of Sustainable Development, Editorial FAN, 2004).44.Werth, S. & Sork, V. L. Ecological specialization in Trebouxia (Trebouxiophyceae) photobionts of Ramalina menziesii (Ramalinaceae) across six range-covering ecoregions of western North America. Am. J. Bot. 101, 1127–1140 (2014).PubMed 
    Article 

    Google Scholar 
    45.Rolshausen, G., Dal Grande, F., Sadowska-Deś, A. D., Otte, J. & Schmitt, I. Quantifying the climatic niche of symbiont partners in a lichen symbiosis indicates mutualistmediated niche expansions. Ecography 41, 1380–1392 (2018).Article 

    Google Scholar 
    46.Blaha, J., Baloch, E. & Grube, M. High photobiont diversity insymbioses of the euryoecious lichen Lecanora rupicola (Lecanoraceae, Ascomycota). Biol. J. Linn. Soc. 88, 283–293 (2006).Article 

    Google Scholar 
    47.Vargas Castillo, R. & Beck, A. Photobiont selectivity and specificity in Caloplaca species in a fog-induced community in the Atacama Desert, northern Chile. Fungal Biol. 116, 665–676 (2012).PubMed 
    Article 

    Google Scholar 
    48.Bačkor, M., Klemová, K., Bačkorová, M. & Ivanova, V. Comparison of the phytotoxic effects of usnic acid on cultures of free-living alga Scenedesmus quadricauda and aposymbiotically grown lichen photobiont Trebouxia erici. J. Chem. Ecol. 36, 405–411 (2010).PubMed 
    Article 
    CAS 

    Google Scholar 
    49.Galloway, D. J. Lichen biogeography. In: Nash T. H. (ed.) Lichen Biology, 315–335 (Cambridge University Press, 2008).50.Dal Grande, F. et al. Environment and host identity structure communities of green algal symbionts in lichens. New Phytol. 217, 277–289 (2017).Article 
    CAS 

    Google Scholar 
    51.Dal Grande, F., Widmer, I., Wagner, H. H. & Scheidegger, C. Vertical and horizontal photobiont transmission within populations of a lichen symbiosis. Mol. Ecol. 21, 3159–3172 (2012).Article 

    Google Scholar 
    52.Otálora, M. A. G. et al. Multiple origins of high reciprocal symbiotic specificity at an intercontinental spatial scale among gelatinous lichens (Collemataceae, Lecanoromycetes). Mol. Phylogenet. Evol. 56, 1089–1095 (2010).PubMed 
    Article 
    CAS 

    Google Scholar 
    53.Ruprecht, U., Fernández-Mendoza, F., Türk, R. & Fryday, A. High levels of endemism and local differentiation in the fungal and algal symbionts of saxicolous lecideoid lichens along a latitudinal gradient in southern South America. Lichenologist 52, 287–303 (2020).PubMed Central 
    Article 
    PubMed 

    Google Scholar 
    54.Ahti, T., Cladoniaceae in Flora Neotropica Monograph 78. 2–362 (New York Botanical Garden Press, 2000).55.Parnmen, S., Leavitt, S. D., Rangsiruji, A. & Lumbsch, H. T. Identification of species in the Cladia aggregata group using DNA barcoding (Ascomycota: Lecanorales). Phytotaxa 115, 1–14 (2013).Article 

    Google Scholar 
    56.Guzow-Krzemińska, B. et al. New species and records of lichens from Bolivia. Phytotaxa 397, 257–279 (2019).Article 

    Google Scholar 
    57.Sipman, H. J. M. Survey of Lepraria species with lobed thallus margins in the tropics. Herzogia 17, 23–35 (2004).
    Google Scholar 
    58.Saag, L., Saag, A. & Randlane, T. World survey of the genus Lepraria (Stereocaulaceae, lichenized Ascomycota). Lichenologist 41, 25–60 (2009).Article 

    Google Scholar 
    59.Guzow-Krzemińska, B. et al. Phylogenetic placement of Lepraria cryptovouauxii sp. nov. (Lecanorales, Lecanoromycetes, Ascomycota) with notes on other Lepraria species from South America. MycoKeys 53, 1–22 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    60.Orange, A., James, P. W. & White, F. J. Microchemical Methods for the Identification of Lichens. 1–101 (British Lichen Society, 2001).61.Cubero, O. F., Crespo, A., Fatehi, J. & Bridge, P. D. DNA extraction and PCR amplification method suitable for fresh, herbarium-stored, lichenized, and other fungi. Plant Syst. Evol. 216, 243–249 (1999).CAS 
    Article 

    Google Scholar 
    62.White, T. J., Bruns, T., Lee, S. & Taylor, J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics in PCR Protocols: A Guide to Methods and Applications (eds Innis, M. A., Gelfand, D. H., Sninsky, J. J. & White, T. J.) 345–322 (Academic Press, 1990).63.Sherwood, A. R., Garbary, D. J. & Sheath, R. G. Assessing the phylogenetic position of the Prasiolales (Chlorophyta) using rbcL and 18S rRNA gene sequence data. Phycologia 39, 139–146 (2000).Article 

    Google Scholar 
    64.Nelsen, M. P., Rivas Plata, E., Andrew, C. J., Lücking, R. & Lumbsch, H. T. Phylogenetic diversity of trentepohlialean algae associated with lichen-forming fungi. J. Phycol. 47, 282–290 (2011).PubMed 
    Article 

    Google Scholar 
    65.Widmer, I., Dal Grande, F., Cornejo, C. & Scheidegger, C. Highly variable microsatellite markers for the fungal and algal symbionts of the lichen Lobaria pulmonaria and challenges in developing biont-specific molecular markers for fungal associations. Fungal Biol. 114, 538–544 (2010).CAS 
    PubMed 
    Article 

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

    Google Scholar 
    67.Katoh, K., Misawa, K., Kuma, K. & Miyata, T. MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059–3066 (2002).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    68.Okonechnikov, K., Golosova, O. & Fursov, M. UGENE team. Unipro GENE: A unified bioinformatics toolkit. Bioinformatics 28, 1166–1167 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    69.Huelsenbeck, J. P. & Ronquist, F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    70.Stamatakis, A. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    71.Chernomor, O., von Haeseler, A. & Minh, B. Q. Terrace aware data structure for phylogenomic inference from supermatrices. Syst. Biol. 65, 997–1008 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    72.Nguyen, L. T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Mol. Biol. Evol. 32, 268–274 (2015).CAS 
    Article 

    Google Scholar 
    73.Miller, M. A., Pfeiffer, W. & Schwartz, T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Gateway Computing Environments Workshop (GCE): 1–8 (2010).74.Lanfear, R., Frandsen, P. B., Wright, A. M., Senfeld, T. & Calcott, B. PartitionFinder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol. Biol. Evol. 34, 772–773 (2016).
    Google Scholar 
    75.Rambaut, A. FigTreev1.4.2. Retrieved from: http://tree.bio.ed.ac.uk/software/figtree/ (2006–2014).76.Oksanen, et al., vegan: Community ecology package manual. Retrieved from https://cran.rproject.org/package=vegan (2017).77.Fick, S. E. & Hijmans, R. J. WorldClim 2: New 1-km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37, 4302–4315 (2017).Article 

    Google Scholar 
    78.Borcard, D., Legendre, P., Avois-Jacquet, C. & Tuomisto, H. Dissecting the spatial structure of ecological data at multiple scales. Ecology 85, 1826–1832 (2004).Article 

    Google Scholar 
    79.Lefeuvre, P. BoSSA: A bunch of structure and sequence analysis manual. Retrieved from https://cran.r-project.org/package=BoSSA (2018).80.McArdle, B. H. & Anderson, M. J. Fitting multivariate models to community data: A comment on distance-based redundancy analysis. Ecology 82, 290–297 (2001).Article 

    Google Scholar 
    81.Stenroos, S., Pino-Bodas, R., Hyvönen, J., Lumbsch, T. H. & Ahti, T. Phylogeny of family Cladoniaceae (Lecanoromycetes, Ascomycota) based on sequences of multiple loci. Cladistics 35, 351–384 (2019).Article 

    Google Scholar 
    82.R Core Team. R: A Language and Environment for Statistical Computing.83.https://www.R-project.org/ (2017).84.RStudio Team. RStudio: Integrated Development for R. RStudio, Inc., Boston, MA URL http://www.rstudio.com/ (2018).85.Aktas, C. Manipulating DNA Sequences and Estimating Unambiguous Haplotype Network with Statistical Parsimony. Retrieved from https://CRAN.R project.org/package=haplotypes (2020).86.Piel, W. H., Chan, L., Dominus, M. J., Ruan, J., Vos, R. A., and V. Tannen. TreeBASE v. 2: A Database of Phylogenetic Knowledge. In: e-BioSphere (2009) More