More stories

  • in

    Effects of climatic factors on the net primary productivity in the source region of Yangtze River, China

    Study area
    The Source Region of Yangtze River (SRYR for short, Latitude: 32° 25′ E and 35° 53′ E; Longitude: 89° 43′ E–97° 19′ E), located in the western Tibetan plateau, covers an area of 141,398 km2 (Fig. 10a). The elevation ranges from 6456 m in the West to 3512 m in the East, with an average of 4779 m. The SRYR belongs to transition zone from semi-arid to semi-humid alpine area. The annual temperature is − 2 to − 3 °C. Monthly mean temperature in the coldest month is − 13.0 °C and that in the warmest month is 9.7 °C. The annual temperature of the study area is 265 mm. The temperature decreases from southeast to northwest37. The aridity index is 3.67 in the SRYR, which means the climate is very dry. The vegetation types are mainly meadow (84,985 km2) and grassland (33,743 km2), which are 60.1% and 23.9% (Fig. 10b) of the study area respectively. We divided the SRYR into five sub-regions, including Tuotuo River Basin (I), Dam River Basin (II), Qumar River Basin (III), Middle Stream Region (IV) and Downstream Region (V).
    Figure 10

    The location of Source Region of Yangtze River (a) and vegetation types (b). Map was generated using ArcGIS 10.3 (http://www.esri.com/software/arcgis/arcgis-for-desktop).

    Full size image

    Datasets
    The monthly NDVI data for SRYR was obtained from Resource and Environment Data Cloud Platform (RESDC, http://www.resdc.cn/). It was produced with Maximum Value Composite (MVC) approach based on the SPOT/VEGETATION NDVI data. The effects of cloud cover and non-vegetation were reduced. This dataset was at a spatial resolution of 1 km, covering the period 2000 to 2014.
    The gridded meteorological data used are obtained from China Ground Precipitation 0.5° × 0.5° Grid Dataset V2.0 and China Ground Temperature 0.5° × 0.5° Grid Dataset V2.0. These datasets are provided by National Meteorological Information Center (NMIC, http://data.cma.cn/). A total of 102 grids in the SRYR and the surroundings during 2000–2014 are selected. The gridded data has been projected and resampled in order to ensure the same coordinate system and resolution with NDVI data. The NMIC also provides meteorological data of 9 meteorological stations within and around the study area, including parameters such as solar radiation, surface water, pressure, sunshine hours, wind speed and relative humidity. Grid data of the study area was interpolated by ANUSPLINE.
    NPP simulation
    In this study, the NPP were simulated by CASA (Carnegie–Ames–Stanford Approach) model. The CASA model is based on the plant growing mechanism38,39,40 which can be summarized by Eq. (1).

    $$ NPPleft( {x,t} right) = APARleft( {x,t} right) times varepsilon left( {x,t} right) $$
    (1)

    where x and t are spatial location and time respectively, NPP is simulated value (gC m−2). APAR and ε represent absorbed photosynthetically active radiation and light use efficiency, which can be obtained by Eqs. (2) and (3).

    $$ APARleft( {x,t} right) = fPARleft( {x,t} right) times SOLleft( {x,t} right) times R $$
    (2)

    $$ varepsilon left( {x,t} right) = Tleft( {x,t} right) times Wleft( {x,t} right) times varepsilon_{max } $$
    (3)

    where fPAR is the fraction of absorbed photosynthetically active radiation, SOL is the total solar radiation (MJ/m2), R is the fraction of solar active radiation that can be used by vegetation. T and W are temperature stress index and moisture stress factor, respectively. εmax is maximum light utilization efficiency. Further details of the above equations can be obtained from previous studies38,39,40.
    The NPP calculated by CASA model can be considered as the actual NPP which is influenced by both climate change and human activities. It can be expressed as Eq. (4).

    $$ NPP = PNPP – HNPP $$
    (4)

    where PNPP and HNPP represent potential NPP and human-induced NPP, respectively. PNPP is only determined by climate conditions and without interference from human activities. It can be calculated by Thornthwaite Memorial model41, using the follows formulas:

    $$ PNPP = 3000left[ {1 – e^{{ – 0.0009695left( {v – 20} right)}} } right] $$
    (5)

    $$ v = frac{1.05N}{{sqrt {1 + left( {1.05{N mathord{left/ {vphantom {N L}} right. kern-nulldelimiterspace} L}} right)^{2} } }} $$
    (6)

    $$ L = 300 + 25t + 0.05t^{3} $$
    (7)

    where t, L, N and v are average annual temperature (°C), annual maximum evapotranspiration (mm), annual total precipitation (mm) and average annual actual evapotranspiration (mm).
    According to Eq. (4), the HNPP can be represented by the difference between PNPP and NPP.
    Statistical analysis
    To identify the inter-annual trends of temperature (Tem.), precipitation (Pre.) and NPP, the linear regression method was adopted to eliminate the increase or decrease rate42, which can be calculated as follows:

    $$ theta_{Slope} = frac{{n times sumnolimits_{i = 1}^{n} {(i times X_{i} ) – sumnolimits_{i = 1}^{n} {isumnolimits_{i = 1}^{n} {X_{i} } } } }}{{n times sumnolimits_{i = 1}^{n} {i^{2} – left( {sumnolimits_{i = 1}^{n} i } right)^{2} } }} $$
    (8)

    where θslope is the linear slope of the time series variable, which can be used to characterize the increase or decrease rate during a given study period; n is the number of years (here n = 15); Xi is the temperature, precipitation and NPP for the ith year (i = 1,2, … n).
    A nonparametric test, Mann–Kendall (M–K) trend analysis43,44 was utilized to detect the break points of temperature, precipitation and NPP series in the SRYR. The test statistic UFi is calculated as follows:

    $$ begin{array}{*{20}c} {UF_{i} = frac{{S_{i} – Eleft( {S_{i} } right)}}{{sqrt {Varleft( {S_{i} } right)} }}} & {left( {i = 1,2, ldots ,n} right)} \ end{array} $$
    (9)

    $$ begin{array}{*{20}c} {S_{k} = sumlimits_{i = 1}^{k} {r_{i} } } & {left( {k = 2,3, ldots ,n} right)} \ end{array} $$
    (10)

    $$ begin{array}{*{20}c} {ri = left{ {begin{array}{*{20}c} { + 1} & {x_{i} > x_{j} } \ 0 & {x_{i} le x_{j} } \ end{array} } right.} & {(j = 1,2, ldots ,i – 1)} \ end{array} $$
    (11)

    where xi is the variable with the sample of n. E(Sk) and variance Var(Sk) could be estimated as follows:

    $$ Eleft( {S_{i} } right) = frac{{ileft( {i – 1} right)}}{4} $$
    (12)

    $$ Varleft( {S_{i} } right) = frac{{ileft( {i – 1} right)left( {2i + 5} right)}}{72} $$
    (13)

    Using the same equation but in the reverse data series (xn, xn − 1, …, x1), UFi could be calculated again. Defining UBi = UFi (i = n, n − 1, …, 1), we can get the curve of UFi and UBi. If the intersection of the UFi and UBi curves occurs within the confidence interval, it indicates a change point45.
    To assess the effects of temperature and precipitation on NPP in the SRYR, correlation coefficient R was employed to analyze the correlation between two variables (NPP vs. Tem., NPP vs. Pre.), using the following formula:

    $$ R_{XY} = frac{{sumnolimits_{i = 1}^{n} {left( {X_{i} – overline{X} } right)left( {Y_{i} – overline{Y} } right)} }}{{sqrt {sumnolimits_{i = 1}^{n} {left( {X_{i} – overline{X} } right)^{2} sqrt {sumnolimits_{i = 1}^{n} {left( {Y_{i} – overline{Y} } right)^{2} } } } } }} $$
    (14)

    where Y denotes the NPP and X denotes temperature or precipitation.
    The results of the statistical analysis above can be got by MATLAB.
    Identification of the relative roles of climate change and human activities in NPP
    A positive PNPP slope indicates that vegetation growth is promoted by climate change, whereas a negative PNPP slope means that climate change reduced the vegetation NPP. A positive HNPP slope suggests that human activities have negative influence on vegetation growth and create ecological degradation, whereas a negative HNPP slope means that human activities contribute to vegetation growth46. Thus, the determinants for NPP change can be identified according to Table 2.
    Table 2 The causes of actual NPPA change.
    Full size table More

  • in

    Temperature driven hibernation site use in the Western barbastelle Barbastella barbastellus (Schreber, 1774)

    1.
    Geiser, F. Metabolic rate and body temperature reduction during hibernation and daily torpor. Annu. Rev. Physiol. 66, 239–274. https://doi.org/10.1146/annurev.physiol.66.032102.115105 (2004).
    ADS  CAS  Article  PubMed  Google Scholar 
    2.
    Speakman, J. R. & Thomas, D. W. In Bat Ecology (eds T. H. Kunz & B. M. Fenton) 430–490 (The University of Chicago Press, 2003).

    3.
    Thomas, D. W., Dorais, M. & Bergeron, J.-M. Winter energy budgets and cost of arousals for hibernating little brown bats, myotis lucifugus. J. Mammal. 71, 475–479. https://doi.org/10.2307/1381967 (1990).
    Article  Google Scholar 

    4.
    Thomas, D. W., Cloutier, D. & Gagné, D. Arrhythmic breathing, apnea and non-steady state oxygen uptake in hibernating Little Brown Bats (Myotis lucifugus). J. Exp. Biol. 149, 395–406 (1990).
    Google Scholar 

    5.
    Hock, R. J. The metabolic rates and body temperatures of bats. Biol. Bull. 101, 289–299 (1951).
    CAS  Article  Google Scholar 

    6.
    McNab, B. K. The behavior of temperate cave bats in a subtropical environment. Ecology 55, 943–958 (1974).
    Article  Google Scholar 

    7.
    Belkin, V. V., Panchenko, D. V., Tirronen, K. F., Yakimova, A. E. & Fedorov, F. V. Ecological status of bats (Chiroptera) in winter roosts in eastern Fennoscandia. Russ. J. Ecol. 46, 463–469. https://doi.org/10.1134/s1067413615050045 (2015).
    Article  Google Scholar 

    8.
    Richter, A. R., Humphrey, S. R., Cope, J. B. & Brack, V. Modified cave entrances – thermal effect on body-mass and resulting decline of endangered indiana bats (Myotis sodalis). Conserv. Biol. 7, 407–415. https://doi.org/10.1046/j.1523-1739.1993.07020407.x (1993).
    Article  Google Scholar 

    9.
    Arlettaz, R. et al. Physiological traits affecting the distribution and wintering strategy of the bat Tadarida teniotis. Ecology 81, 1004–1014. https://doi.org/10.1890/0012-9658(2000)081[1004:ptatda]2.0.co;2 (2000).
    Article  Google Scholar 

    10.
    Clawson, R. L., Laval, R. K., Laval, M. L. & Caire, W. Clustering behaviour of hibernating Myotis Sodalis in Missouri. J. Mammal. 61, 245–253. https://doi.org/10.2307/1380045 (1980).
    Article  Google Scholar 

    11.
    McManus, J. J. Activity and thermal preference of the little brown bat, Myotis lucifugus, during hibernation. J. Mammal. 55, 844–846 (1974).
    CAS  Article  Google Scholar 

    12.
    Ingersoll, T. E., Navo, K. W. & de Valpine, P. Microclimate preferences during swarming and hibernation in the Townsend’s big-eared bat, Corynorhinus townsendii. J. Mammal. 91, 1242–1250. https://doi.org/10.1644/09-mamm-a-288.1 (2010).
    Article  Google Scholar 

    13.
    Webb, P. I., Speakman, J. R. & Racey, P. A. How hot is a hibernaculum? A review of the temperatures at which bats hibernate. Can. J. Zool.-Rev. Can. Zool. 74, 761–765. https://doi.org/10.1139/z96-087 (1996).
    Article  Google Scholar 

    14.
    Gaisler, J. Remarks on the thermopreferendum of palearctic bats in their natural habitats. Bijdragen tot de Dierkunde 40, 33–35 (1970).
    Article  Google Scholar 

    15.
    Bogdanowicz, W. & Urbanczyk, Z. Some ecological aspects of bats hibernating in the city of Poznan. Acta Theriologica 28, 371–385 (1983).
    Article  Google Scholar 

    16.
    Lesinski, G. Ecology of bats hibernating underground in Central Poland. Acta Theriologica 31, 507–521 (1986).
    Article  Google Scholar 

    17.
    Nagel, A. & Nagel, R. How do bats choose optimal temperatures for hibernation?. Comp. Biochem. Physiol. A Physiol. 99, 323–326. https://doi.org/10.1016/0300-9629(91)90008-Z (1991).
    Article  Google Scholar 

    18.
    Siivonen, Y. & Wermundsen, T. Characteristics of winter roosts of bat species in southern Finland. Mammalia 72, 50–56. https://doi.org/10.1515/mamm.2008.003 (2008).
    Article  Google Scholar 

    19.
    Brack, V. Jr. Temperatures and locations used by hibernating bats, including Myotis sodalis (Indiana bat), in a limestone mine: Implications for conservation and management. Environ. Manag. 40, 739–746. https://doi.org/10.1007/s00267-006-0274-y (2007).
    ADS  MathSciNet  Article  Google Scholar 

    20.
    Boyles, J. G., Johnson, J. S., Blomberg, A. & Lilley, T. M. Optimal hibernation theory. Mammal Rev. 50, 91–100. https://doi.org/10.1111/mam.12181 (2020).
    Article  Google Scholar 

    21.
    Prendergast, B. J., Freeman, D. A., Zucker, I. & Nelson, R. J. Periodic arousal from hibernation is necessary for initiation of immune responses in ground squirrels. Am. J. Physiol.-Regul. Integr. Comp. Physiol. 282, R1054–R1062. https://doi.org/10.1152/ajpregu.00562.2001 (2002).
    CAS  Article  PubMed  Google Scholar 

    22.
    Burton, R. S. & Reichman, O. J. Does immune challenge affect torpor duration?. Funct. Ecol. 13, 232–237. https://doi.org/10.1046/j.1365-2435.1999.00302.x (1999).
    Article  Google Scholar 

    23.
    Daan, S., Barnes, B. M. & Strijkstra, A. M. Warming up for sleep? Ground-squirrels sleep during arousals from hibernation. Neurosci. Lett. 128, 265–268. https://doi.org/10.1016/0304-3940(91)90276-y (1991).
    CAS  Article  PubMed  Google Scholar 

    24.
    van Breukelen, F. & Martin, S. L. Molecular biology of thermoregulation – Invited review: molecular adaptations in mammalian hibernators: unique adaptations or generalized responses?. J. Appl. Physiol. 92, 2640–2647. https://doi.org/10.1152/japplphysiol.01007.2001 (2002).
    Article  PubMed  Google Scholar 

    25.
    Kokurewicz, T. Sex and age related habitat selection and mass dynamics of Daubenton’s bats Myotis daubentonii (Kuhl, 1817) hibernating in natural conditions. Acta Chiropterologica 6, 121–144 (2004).
    Article  Google Scholar 

    26.
    Czenze, Z. J., Jonasson, K. A. & Willis, C. K. R. Thrifty females, frisky males: winter energetics of hibernating bats from a cold climate. Physiol. Biochem. Zool. 90, 502–511. https://doi.org/10.1086/692623 (2017).
    Article  PubMed  Google Scholar 

    27.
    Boyles, J. G., Dunbar, M. B., Storm, J. J. & Brack, V. Jr. Energy availability influences microclimate selection of hibernating bats. J. Exp. Biol. 210, 4345–4350. https://doi.org/10.1242/jeb.007294 (2007).
    Article  PubMed  Google Scholar 

    28.
    Daan, S. & Wichers, H. J. Habitat selection of bats hibernating in a limestone cave. Z. Fur Saugetierkunde-Int. J. Mammalian Biol. 33, 262–287 (1968).

    29.
    Daan, S. Activity during natural hibernation in three species of vespertilionid bats. Netherlands J. Zool. 23, 1–71 (1973).
    Article  Google Scholar 

    30.
    Kirkpatrick, L., Apoznanski, G., De Bruyn, L., Gyselings, R. & Kokurewicz, T. Bee markers: a novel method for non invasive short term marking of bats. Acta Chiropterologica 21, 465–471. https://doi.org/10.3161/15081109acc2019.21.2.020 (2019).
    Article  Google Scholar 

    31.
    Bagrowska-Urbanczyk, E. & Urbanczyk, Z. Structure and dynamics of a winter colony of bats. Acta Theriologica 28, 183–196 (1983).
    Article  Google Scholar 

    32.
    Boyles, J. G., Boyles, E., Dunlap, R. K., Johnson, S. A. & Brack, V. Long-term microclimate measurements add further evidence that there is no “optimal” temperature for bat hibernation. Mammalian Biol. 86, 9–16. https://doi.org/10.1016/j.mambio.2017.03.003 (2017).
    Article  Google Scholar 

    33.
    Boyles, J. G. & McKechnie, A. E. Energy conservation in hibernating endotherms: why “suboptimal” temperatures are optimal. Ecol. Model. 221, 1644–1647. https://doi.org/10.1016/j.ecolmodel.2010.03.018 (2010).
    Article  Google Scholar 

    34.
    Webb, P. I., Speakman, J. R. & Racey, P. A. Population dynamics of a maternity colony of the pipistrelle bat (Pipistrellus pipistrellus) in north-east Scotland. J. Zool. 240, 777–780. https://doi.org/10.1111/j.1469-7998.1996.tb05323.x (1996).
    Article  Google Scholar 

    35.
    IPCC. Climate Change 2007: Impacts, Adaptation and Vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Eds. Parry, M., Canziani, M., Palutikof, O., van der Linden, J., Hanson, P., Cambridge, C., (Cambridge University Press, 2007).

    36.
    Lutenbacher, J., Dietrich, D., Xoplaki, E., Grosjean, M. & Wanner, H. European seasonal and annual temperature variability, trends, and extremes since 1500. Science 303, 1499–1503 (2004).
    ADS  Article  Google Scholar 

    37.
    Piniewski, M., Mezghani, A., Szcześniak, M. & Kundzewicz, Z. W. Regional projections of temperature and precipitation changes: robustness and uncertainty aspects. Meteorol. Z. 26, 223–234. https://doi.org/10.1127/metz/2017/0813 (2017).
    Article  Google Scholar 

    38.
    Humphries, M. M., Thomas, D. W. & Speakman, J. R. Climate-mediated energetic constraints on the distribution of hibernating mammals. Nature 418, 313–316. https://doi.org/10.1038/nature00828 (2002).
    ADS  CAS  Article  PubMed  Google Scholar 

    39.
    Day, K. M. & Tomasi, T. E. Winter energetics of female Indiana bats Myotis sodalis. Physiol. Biochem. Zool. 87, 56–64. https://doi.org/10.1086/671563 (2014).
    Article  PubMed  Google Scholar 

    40.
    Rebelo, H., Tarroso, P. & Jones, G. Predicted impact of climate change on European bats in relation to their biogeographic patterns. Glob. Change Biol. 16, 561–576. https://doi.org/10.1111/j.1365-2486.2009.02021.x (2010).
    ADS  Article  Google Scholar 

    41.
    Gottfried, I. et al. Long-term changes in winter abundance of the barbastelle Barbastella barbastellus in Poland and the climate change: are current monitoring schemes still reliable for cryophilic bat species?. PLoS ONE 15, 18. https://doi.org/10.1371/journal.pone.0227912 (2020).
    CAS  Article  Google Scholar 

    42.
    Rydell, J. & Bogdanowicz, W. Barbastella barbastellus. Mammalian Species, 1–8 (1997).

    43.
    Lesinski, G. et al. The importance of small cellars to bat hibernation in Poland. Mammalia 68, 345–352. https://doi.org/10.1515/mamm.2004.034 (2004).
    Article  Google Scholar 

    44.
    Sachanowicz, K. & Zub, K. Numbers of hibernating Barbastella barbastellus (Schreber, 1774) (Chiroptera, Vespertilionidae) and thermal conditions in military bunkers. Mammalian Biol. 67, 179–184. https://doi.org/10.1078/1616-5047-00026 (2002).
    Article  Google Scholar 

    45.
    Greenaway, F. The barbastelle in Britain. British Wildlife 12, 327–334 (2001).
    Google Scholar 

    46.
    Sherwin, H. A., Montgomery, W. I. & Lundy, M. G. The impact and implications of climate change for bats. Mammal Rev. 43, 171–182. https://doi.org/10.1111/j.1365-2907.2012.00214.x (2013).
    Article  Google Scholar 

    47.
    Dietz, C., Von Helversen, O. & Nill, D. Bats of Britain, Europe & Northwest Africa. (A &C Black Publishers Ltd., 2009).

    48.
    Hutterer, R., Ivanova, T., Meyer-Cords, C. & Rodrigues, L. Bat migrations in Europe: a review of banding data and literature. Vol. 28 (Federal Agency for Nature Conservation in Germany, 2005).

    49.
    Kokurewicz, T. et al. 45 years of bat study and conservation in Nietoperek bat reserve (Western Poland). Nyctalus 19, 252–269 (2019).
    Google Scholar 

    50.
    Cichocki, J. et al. In 23th Polish Chiropterological Conference. (ed W. Grzywinski) 9–10 (2014).

    51.
    Cichocki, J. et al. In Proceedings of the 24th Polish Chiropterological Conference. (ed W. Grzywinski) 36–37 (2015).

    52.
    Brack, V. & Twente, J. W. The duration of the period of hibernationof 3 species of Vespertilionid bats. 1. Field studies. Can. J. Zool.-Rev. Can. Zool. 63, 2952–2954 (1985).

    53.
    Zuur, A. F., Ieno, E. N., Walker, N. J., Saveliev, A. A. & Smith, G. M. Mixed effects models and extensions in ecology with R. (Springer, 2009).

    54.
    Onkelinx, T., Devos, K. & Quataert, P. Working with population totals in the presence of missing data comparing imputation methods in terms of bias and precision. J. Ornithol. 158, 603–615. https://doi.org/10.1007/s10336-016-1404-9 (2017).
    Article  Google Scholar 

    55.
    Rubin, D. B. Multiple Imputation for Nonresponse in Surveys. (Wiley, 1987).

    56.
    Rubin, D. B. Multiple imputation after 18+ years. J. Am. Stat. Assoc. 91, 473–489. https://doi.org/10.1080/01621459.1996.10476908 (1996).
    Article  MATH  Google Scholar 

    57.
    RCoreTeam. in Version 3.6.1 (URL https://www.R-project.org/: R Foundation for Statistical Computing, Vienna, Austria, 2019).

    58.
    Mixed GAM Computation Vehicle with GCV/AIC/REML smoothness estimation v. 1.8–0 (2014).

    59.
    Venables, W. N. & Ripley, B. D. Modern Applied Statistics with S. Fourth Edition. (Springer, 2002).

    60.
    Tuttle, M. D. & Stevenson, D. E. in BCI Bat Conservation and Management Workshop. 19–35 (Bat Conservation International).

    61.
    Lesinski, G., Fuszara, E., Fuszara, M., Jurczyszyn, M. & Urbanczyk, Z. Long-term changes in the numbers of the barbastelle Barbastella barbastellus in Poland. Folia Zool. 54, 351–358 (2005).
    Google Scholar 

    62.
    Klug-Baerwald, B. J., Lausen, C. L., Willis, C. K. R. & Brigham, R. M. Home is where you hang your bat: winter roost selection by prairie-living big brown bats. J. Mammal. 98, 752–760. https://doi.org/10.1093/jmammal/gyx039 (2017).
    Article  Google Scholar 

    63.
    Martinkova, N., Baird, S. J. E., Kana, V. & Zima, J. Bat population recoveries give insight into clustering strategies during hibernation. Front. Zool. 17, 11. https://doi.org/10.1186/s12983-020-00370-0 (2020).
    Article  Google Scholar 

    64.
    Tuttle, M. D. & Kennedy, J. In BCI Bat Conservation and Management Workshop. 73–82 (Bat Conservation International).

    65.
    Suggitt, A. J. et al. Extinction risk from climate change is reduced by microclimatic buffering. Nat. Climate Change 8, 713–717. https://doi.org/10.1038/s41558-018-0231-9 (2018).
    ADS  Article  Google Scholar 

    66.
    Thomas, D. W. Hibernating bats are sensitive to nontactile human disturbance. J. Mammal. 76, 940–946. https://doi.org/10.2307/1382764 (1995).
    Article  Google Scholar 

    67.
    Speakman, J. R., Webb, P. I. & Racey, P. A. Effects of disturbance on the energy expenditure of hibernating bats. J. Appl. Ecol. 28, 1087–1104. https://doi.org/10.2307/2404227 (1991).
    Article  Google Scholar 

    68.
    Jurga, R. M. & Kędryna A. M. Festungsfront Oder-Warthe Bogen. Katalog (Wydawnictwo Donjon, 2006). More

  • in

    The role of the brown bear Ursus arctos as a legitimate megafaunal seed disperser

    1.
    Cain, M. L., Milligan, B. G. & Strand, A. E. Long-distance seed dispersal in plant populations. Am. J. Bot. 87, 1217–1227 (2000).
    CAS  PubMed  PubMed Central  Article  Google Scholar 
    2.
    Cousens, R., Dytham, C. & Law, R. Dispersal in Plants: A Population Perspective 1st edn. (Oxford University Press, Oxford, 2008).
    Google Scholar 

    3.
    Jordano, P. Fruits and frugivory. In Seeds: The Ecology of Regeneration in Plant Communities 2nd edn (ed. Fenner, M.) 125–166 (UK CAB International, Wallingford, 2000).
    Google Scholar 

    4.
    Jordano, P., García, C., Godoy, J. A. & García-Castaño, J. L. Differential contribution of frugivores to complex seed dispersal patterns. PNAS 104, 3278–3282 (2007).
    CAS  PubMed  Article  ADS  Google Scholar 

    5.
    Bueno, R. S. et al. Functional redundancy and complementarities of seed dispersal by the last neotropical megafrugivores. PLoS ONE 8, 0056252 (2013).
    Article  ADS  CAS  Google Scholar 

    6.
    Pérez-Méndez, N., Jordano, P., García, C. & Valido, A. The signatures of Anthropocene defaunation: cascading effects of the seed dispersal collapse. Sci. Rep. 6, 24820 (2016).
    PubMed  PubMed Central  Article  ADS  CAS  Google Scholar 

    7.
    Hamrick, J. L., Murawski, D. A. & Nason, J. D. The influence of seed dispersal mechanisms on the genetic structure of tropical tree populations. Vegetatio 107, 281–297 (1993).
    Google Scholar 

    8.
    Mueller, T., Lenz, J., Caprano, T., Fiedler, W. & Böhning-Gaese, K. Large frugivorous birds facilitate functional connectivity of fragmented landscapes. J. Appl. Ecol. 51, 684–692 (2014).
    Article  Google Scholar 

    9.
    Pérez-Méndez, N., Jordano, P. & Valido, A. Persisting in defaunated landscapes: reduced plant population connectivity after seed dispersal collapse. J. Ecol. 106, 936–947 (2018).
    Article  Google Scholar 

    10.
    Schupp, E. W. Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio 107, 15–29 (1993).
    Google Scholar 

    11.
    Schupp, E. W., Jordano, P. & Gómez, J. M. Seed dispersal effectiveness revisited: a conceptual review. New Phytol. 188, 333–353 (2010).
    PubMed  Article  Google Scholar 

    12.
    Traveset, A. & Richardson, D. M. Mutualistic interactions and biological invasions. Annu. Rev. Ecol. Evol. Syst. 45, 89–113 (2014).
    Article  Google Scholar 

    13.
    Herrera, C. M. Seed dispersal by vertebrates. In Plant—animal interactions, an evolutionary approach (eds Herrera, C. & Pellmyr, O.) 185–209 (Wiley, Oxford, 2002).
    Google Scholar 

    14.
    Vidal, M. M., Pires, M. M. & Guimarães, J. P. R. Large vertebrates as the missing components of seed-dispersal networks. Biol. Conserv. 163, 42–48 (2013).
    Article  Google Scholar 

    15.
    Moleón, M. et al. Rethinking megafauna. Proc. R. Soc. B 287, 20192643 (2020).
    PubMed  Article  Google Scholar 

    16.
    Pires, M. M., Guimarães, P. R., Galetti, M. & Jordano, P. Pleistocene megafaunal extinctions and the functional loss of long-distance seed-dispersal services. Ecography 41, 153–163 (2018).
    Article  Google Scholar 

    17.
    Chen, S. C. & Moles, A. T. A mammoth mouthful? A test of the idea that larger animals ingest larger seeds. Glob. Ecol. Biogeogr. 24, 1269–1280 (2015).
    Article  Google Scholar 

    18.
    Dirzo, R. et al. Defaunation of the anthropocene. Science 345, 401–406 (2014).
    CAS  PubMed  Article  ADS  Google Scholar 

    19.
    Galetti, M. et al. Functional extinction of birds drives rapid evolutionary changes in seed size. Science 340, 1086–1090 (2013).
    CAS  PubMed  Article  ADS  Google Scholar 

    20.
    Pasitschniak-Arts, M. Ursus arctos. Mamm. Species 439, 1–10 (1993).
    Article  Google Scholar 

    21.
    Steyaert, S. M. J. G., Endrestøl, A., Hacklaender, K., Swenson, J. E. & Zedrosser, A. The mating system of the brown bear Ursus arctos. Mamm. Rev. 42, 12–34 (2012).
    Article  Google Scholar 

    22.
    Bojarska, K. & Selva, N. Spatial patterns in brown bears Ursus arctos diet: the role of geographical and environmental factors. Mamm. Rev. 42, 120–143 (2012).
    Article  Google Scholar 

    23.
    Blanchard, B. N. Size and growth patterns of the Yellowstone grizzly bear. Bears Their Biol. Manag. 7, 99–107 (1987).
    Article  Google Scholar 

    24.
    Palomero, G., Fernández-Gil, A. & Naves, J. Reproductive rates of brown bears in the Cantabrian Mountains, Spain. Bears Their Biol. Manag. 9, 129–132 (1997).
    Article  Google Scholar 

    25.
    Welch, C. A., Keay, J., Kendall, K. C. & Robbins, C. T. Constraints on frugivory by bears. Ecology 78, 1105–1119 (1997).
    Article  Google Scholar 

    26.
    Hilderbrand, G. V. et al. The importance of meat, particularly salmon, to body size, population productivity, and conservation of North American brown bears. Can. J. Zool. 77, 132–138 (1999).
    Article  Google Scholar 

    27.
    McLoughlin, P. D., Ferguson, S. H. & Messier, F. Intraspecific variation in home range overlap with habitat quality: a comparison among brown bear populations. Evol. Ecol. 14, 39–60 (2000).
    Article  Google Scholar 

    28.
    Nomura, F. & Higashi, S. Effects of food distribution on the habitat usage of a female brown bear Ursus arctos yesoensis in a beech-forest zone of northernmost Japan. Ecol. Res. 15, 209–217 (2000).
    Article  Google Scholar 

    29.
    Hertel, A. G. et al. Berry production drives bottom-up effects on body mass and reproductive success in an omnivore. Oikos 127, 197–207 (2017).
    Article  Google Scholar 

    30.
    Zalewski, A. Geographical and seasonal variation in food habits and prey size of European pine martens. In Gilbert Martens and Fishers (Martes) in Human-Altered Environments (eds Harrison, D. J. & Fuller, A. K. P.) 77–98 (Springer, Boston, 2005).
    Google Scholar 

    31.
    Soe, E. et al. Europe-wide biogeographical patterns in the diet of an ecologically and epidemiologically important mesopredator, the red fox Vulpes vulpes: a quantitative review. Mamm. Rev. 47, 198–211 (2017).
    Article  Google Scholar 

    32.
    Jaroszewicz, B., Pirożnikow, E. & Sondej, I. Endozoochory by the guild of ungulates in Europe’s primeval forest. Forest Ecol. Manag. 305, 21–28 (2013).
    Article  Google Scholar 

    33.
    Lundgren, E. J., Ramp, D., Ripple, W. J. & Wallach, A. D. Introduced megafauna are rewilding the Anthropocene. Ecography 41, 857–866 (2018).
    Article  Google Scholar 

    34.
    Kowalczyk, R. et al. Foraging plasticity allows a large herbivore to persist in a sheltering forest habitat: DNA metabarcoding diet analysis of the European bison. Forest Ecol. Manag. 449, 117474 (2019).
    Article  Google Scholar 

    35.
    Gebert, C. & Verheyden-Tixier, H. Variation of diet composition of red deer (Cervus elaphus L.) in Europe. Mamm. Rev. 31, 189–201 (2008).
    Article  Google Scholar 

    36.
    Cosyns, E., Delporte, A., Lens, L. & Hoffmann, M. Germination success of temperate grassland species after gut passage through ungulate and rabbit guts. J. Ecol. 93, 353–361 (2005).
    Article  Google Scholar 

    37.
    Albrecht, J. et al. Humans and climate change drove the Holocene decline of the brown bear. Sci. Rep. 7, 1–11 (2017).
    CAS  Article  Google Scholar 

    38.
    Hertel, A. G. et al. Bears and berries: species-specific selective foraging on a patchily distributed food resource in a human-altered landscape. Behav. Ecol. Sociobiol. 70, 831–842 (2016).
    PubMed  PubMed Central  Article  Google Scholar 

    39.
    Valido, A., Schaefer, H. M. & Jordano, P. Colour, design and reward: phenotypic integration of fleshy fruit displays. J. Evol. Biol. 24, 751–760 (2011).
    CAS  PubMed  Article  Google Scholar 

    40.
    MacHutchon, A. G. & Wellwood, D. W. Grizzly bear food habits in the northern Yukon, Canada. Ursus 14, 225–235 (2003).
    Google Scholar 

    41.
    Sato, Y., Mano, T. & Takatsuki, S. Stomach contents of brown bears Ursus arctos in Hokkaido, Japan. Wildl. Biol. 11, 133–144 (2005).
    Article  Google Scholar 

    42.
    Lalleroni, A., Quenette, P.-Y., Daufresne, T., Pellerin, M. & Baltzinger, C. Exploring the potential of brown bear (Ursus arctos) as a long-distance seed disperser: a pilot study in South-Western Europe. Mammalia 81, 1–9 (2017).
    Article  Google Scholar 

    43.
    Baldwin, R. A. & Bender, L. C. Foods and nutritional components of diets of black bear in Rocky Mountain National Park, Colorado. Can. J. Zool. 87, 1000–1008 (2009).
    CAS  Article  Google Scholar 

    44.
    Koike, S. Long-term trends in food habits of Asiatic black bears in the Misaka Mountains on the Pacific coast of central Japan. Mamm. Biol. 75, 17–28 (2010).
    Article  Google Scholar 

    45.
    Campos-Arceiz, A. & Blake, S. Megagardeners of the forest—the role of elephants in seed dispersal. Acta Oecol. 37, 542–553 (2011).
    Article  ADS  Google Scholar 

    46.
    Willson, M. F. & Gende, S. M. Seed dispersal by brown bears, Ursus arctos, in southeastern Alaska. Can. Field-Nat. 118, 499–503 (2004).
    Article  Google Scholar 

    47.
    Naoe, S. et al. Mountain-climbing bears protect cherry species from global warming through vertical seed dispersal. Curr. Biol. 26, 315–316 (2016).
    Article  CAS  Google Scholar 

    48.
    Naoe, S. et al. Downhill seed dispersal by temperate mammals: a potential threat to plant escape from global warming. Sci. Rep. 9, 1–11 (2019).
    CAS  Article  Google Scholar 

    49.
    McConkey, K. R. & O’Farrill, G. Loss of seed dispersal before the loss of seed dispersers. Biol. Conserv. 201, 38–49 (2016).
    Article  Google Scholar 

    50.
    Skuban, M., Finďo, S. & Kajba, M. Human impacts on bear feeding habits and habitat selection in the Poľana Mountains, Slovakia. Eur. J. Wildl. Res. 62, 353–364 (2016).
    Article  Google Scholar 

    51.
    Štofík, J., Merganič, J., Merganičová, K., Bučko, J. & Saniga, M. Brown bear winter feeding ecology in the area with supplementary feeding—Eastern Carpathians (Slovakia). Pol. J. Ecol. 64, 277–288 (2016).
    Article  Google Scholar 

    52.
    Selva, N. et al. Supplementary ungulate feeding affects movement behavior of brown bears. Basic Appl. Ecol. 24, 68–76 (2017).
    Article  Google Scholar 

    53.
    López-Bao, J. V. & González-Varo, J. P. Frugivory and spatial patterns of seed deposition by carnivorous mammals in anthropogenic landscapes: a multi-scale approach. PLoS ONE 6, e14569 (2011).
    PubMed  PubMed Central  Article  ADS  CAS  Google Scholar 

    54.
    Traveset, A. & Willson, M. F. Effect of birds and bears on seed germination of fleshy-fruited plants in temperate rainforests of southeast Alaska. Oikos 80, 89–95 (1997).
    Article  Google Scholar 

    55.
    Nowak, J. & Crone, E. E. It is good to be eaten by a bear: effects of ingestion on seed germination. Am. Midl. Nat. 167, 205–209 (2012).
    Article  Google Scholar 

    56.
    Steyaert, S. M. J. G., Hertel, A. G. & Swenson, J. E. Endozoochory by brown bears stimulates germination in bilberry. Wildl. Biol. 2019, wlb.00573 (2019).
    Article  Google Scholar 

    57.
    Samuels, I. A. & Levey, D. J. Effects of gut passage on seed germination: do experiments answer the questions they ask?. Funct. Ecol. 19, 365–368 (2005).
    Article  Google Scholar 

    58.
    Valido, A. & Olesen, J. M. The importance of lizards as frugivores and seed dispersers. In Seed Dispersal: Theory and its Application in a Changing World (eds Dennis, A. J. et al.) 124–147 (CAB International, Wallingford, 2007).
    Google Scholar 

    59.
    Traveset, A. Effect of seed passage through vertebrate frugivores’ guts on germination: a review. Perspect. Plant. Ecol. Syst. 1, 151–190 (1998).
    Article  Google Scholar 

    60.
    Eriksson, O. & Fröborg, H. “Windows of opportunity” for recruitment in long-lived clonal plants: experimental studies of seedling establishment in Vaccinium shrubs. Can J. Bot. 74, 1369–1374 (1996).
    Article  Google Scholar 

    61.
    Jansen, P. A. et al. Thieving rodents as substitute dispersers of megafaunal seeds. PNAS 109, 12610–12615 (2012).
    CAS  PubMed  Article  ADS  PubMed Central  Google Scholar 

    62.
    Koike, S. et al. Seed removal and survival in Asiatic black bears Ursus thibetanus scats: effect of rodents as secondary seed dispersers. Wildlife Biol. 18, 24–34 (2012).
    Article  Google Scholar 

    63.
    Bartoń, K. A., Zwijacz-Kozica, T., Zięba, F., Sergiel, A. & Selva, N. Bears without borders: long-distance movement in human-dominated landscapes. Glob. Ecol. Conserv. 17, e00541 (2019).
    Article  Google Scholar 

    64.
    Willson, M. F. & Traveset, A. The ecology of seed dispersal. In Seeds: The Ecology of Regeneration in Plant Communities 2nd edn (ed. Fenner, M.) 85–111 (CAB International, Wallingford, 2000).
    Google Scholar 

    65.
    Elfström, M., Støen, O.-G., Zedrosser, A., Warrington, I. & Swenson, J. E. Gut retention times in captive brown bears Ursus arctos. Wildl. Biol. 19, 317–324 (2013).
    Article  Google Scholar 

    66.
    Koike, S. et al. Estimate of the seed shadow created by the Asiatic black bear Ursus thibetanus and its characteristics as a seed disperser in Japanese cool-temperate forest. Oikos 120, 280–290 (2010).
    Article  Google Scholar 

    67.
    Hickey, J. R., Flynn, R. W., Buskirk, S. W., Gerow, K. G. & Willson, M. F. An evaluation of a mammalian predator, Martes americana, as a disperser of seeds. Oikos 87, 499–508 (1999).
    Article  Google Scholar 

    68.
    Terakawa, M., Isagi, Y., Matsui, K. & Yumoto, T. Microsatellite analysis of the maternal origin of Myrica rubra seeds in the feces of Japanese macaques. Ecol. Res. 24, 663–670 (2009).
    CAS  Article  Google Scholar 

    69.
    González-Varo, J. P., López-Bao, J. V. & Guitián, J. Functional diversity among seed dispersal kernels generated by carnivorous mammals. J. Anim. Ecol. 82, 562–571 (2013).
    PubMed  Article  Google Scholar 

    70.
    Tsuji, Y., Okumura, T., Kitahara, M. & Jiang, Z. Estimated seed shadow generated by Japanese martens (Martes melampus): comparison with forest-dwelling animals in Japan. Zool. Sci. 33, 352–357 (2016).
    Article  Google Scholar 

    71.
    Santini, L. et al. Ecological correlates of dispersal distance in terrestrial mammals. Hystrix 24, 181–186 (2013).
    Google Scholar 

    72.
    Bunney, K., Bond, W. J. & Henley, M. Seed dispersal kernel of the largest surviving megaherbivore—the African savanna elephant. Biotropica 49, 395–401 (2017).
    Article  Google Scholar 

    73.
    Galetti, et al. Ecological and evolutionary legacy of megafauna extinctions. Biol. Rev. 93, 845–862 (2018).
    PubMed  Article  Google Scholar 

    74.
    Olson, D. M. et al. Terrestrial ecoregions of the world: a new map of life on earth: a new global map of terrestrial ecoregions provides an innovative tool for conserving biodiversity. Bioscience 51, 933–938 (2001).
    Article  Google Scholar 

    75.
    Nin, S., Petrucci, W. A., Del Bubba, M., Ancillotti, C. & Giordani, E. Effects of environmental factors on seed germination and seedling establishment in bilberry (Vaccinium myrtillus L.). Sci. Hortic. 226, 241–249 (2017).
    Article  Google Scholar 

    76.
    Bates, D., Maechler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).
    Article  Google Scholar 

    77.
    Oksanen, J. et al. Vegan package: community ecology package. R package version 2.5–6 (2019).

    78.
    Silva, L. J. D. & Medeiros, A. D. D. SeedCalc, a new automated R software tool for germination and seedling length data processing. J. Seed. Sci. 41, 250–257 (2019).
    Article  Google Scholar 

    79.
    R Development Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ (2017).

    80.
    South, A. rworldmap: a new R package for mapping global data. R J. 3, 35–43 (2011).
    Article  Google Scholar 

    81.
    IUCN SSC Bear Specialist Group. Ursus arctos. The IUCN Red List of Threatened Species. Version 2017-3 (2017). http://www.iucnredlist.org (Downloaded in May 2020). More

  • in

    Drivers of spatio-temporal variation in mosquito submissions to the citizen science project ‘Mückenatlas’

    1.
    Paupy, C., Delatte, H., Bagny, L., Corbel, V. & Fontenille, D. Aedes albopictus, an arbovirus vector: From the darkness to the light. Microbes Infect. 11, 1177–1185 (2009).
    CAS  PubMed  Article  Google Scholar 
    2.
    Scholte, E. J. & Schaffner, F. Waiting for the tiger: Establishment and spread of the Aedes albopictus mosquito in Europe. In Emerging Pests and Vector-Borne Diseases in Europe (eds Takken, W. & Knols, B. G. J.) 241–260 (Wageningen Academic Publishers, Wageningen, 2007).
    Google Scholar 

    3.
    Kraemer, M. U. G. et al. Past and future spread of the arbovirus vectors Aedes aegypti and Aedes albopictus. Nat. Microbiol. 4, 854–863. https://doi.org/10.1038/s41564-019-0376-y (2019).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    4.
    Kuhlisch, C., Kampen, H. & Walther, D. The Asian tiger mosquito Aedes albopictus (Diptera: Culicidae) in Central Germany: Surveillance in its northernmost distribution area. Acta Trop. 188, 78–85 (2018).
    PubMed  Article  PubMed Central  Google Scholar 

    5.
    Kampen, H. & Walther, D. Vector potential of mosquito species (Diptera: Culicidae) occurring in Central Europe. In Mosquito-borne Diseases: Implications for Public Health, Parasitol. Res. Monogr. Vol. 10 (eds Benelli, G. & Mehlhorn, H.) 41–68 (Springer, Heidelberg, 2018).
    Google Scholar 

    6.
    Kampen, H., Schuhbauer, A. & Walther, D. Emerging mosquito species in Germany—A synopsis after 6 years of mosquito monitoring (2011–2016). Parasitol. Res. 116, 3253–3263 (2017).
    PubMed  Article  PubMed Central  Google Scholar 

    7.
    Ziegler, U. et al. West Nile virus epidemic in Germany triggered by epizootic emergence, 2019. Viruses 12, 448. https://doi.org/10.3390/v12040448 (2020).
    Article  PubMed Central  Google Scholar 

    8.
    Sullivan, B. L. et al. The eBird enterprise: An integrated approach to development and application of citizen science. Biol. Conserv. 169, 31–40 (2014).
    Article  Google Scholar 

    9.
    Oltra, A., Palmer, J. R. B. & Bartumeus, F. AtrapaelTigre.com: Enlisting citizen-scientists in the war on tiger mosquitoes. In European Handbook of Crowdsourced Geographic Information (eds Capineri, C. et al.) 295–308 (Ubiquity Press, London, 2016).
    Google Scholar 

    10.
    Heigl, F., Horvath, K., Laaha, G. & Zaller, J. G. Amphibian and reptile road-kills on tertiary roads in relation to landscape structure: Using a citizen science approach with open-access land cover data. BMC Ecol. 17, 24. https://doi.org/10.1186/s12898-017-0134-z (2017).
    Article  PubMed  PubMed Central  Google Scholar 

    11.
    Walther, D. & Kampen, H. The citizen science project “Mueckenatlas” helps monitor the distribution and spread of invasive mosquito species in Germany. J. Med. Entomol. 54, 1790–1794 (2017).
    PubMed  PubMed Central  Article  Google Scholar 

    12.
    Pocock, M. J. O., Roy, H. E., Fox, R., Ellis, W. N. & Botham, M. Citizen science and invasive alien species: Predicting the detection of the oak processionary moth Thaumetopoea processionea by moth recorders. Biol. Conserv. 208, 146–154 (2017).
    Article  Google Scholar 

    13.
    Kampen, H., Kronefeld, M., Zielke, D. & Werner, D. Further specimens of the Asian tiger mosquito Aedes albopictus (Diptera, Culicidae) trapped in Southwest Germany. Parasitol. Res. 112, 905–907 (2013).
    PubMed  Article  PubMed Central  Google Scholar 

    14.
    Kampen, H., Kuhlisch, C., Fröhlich, A., Scheuch, D. E. & Walther, D. Occurrence and spread of the invasive Asian bush mosquito Aedes japonicus japonicus (Diptera: Culicidae) in West and North Germany since detection in 2012 and 2013, respectively. PLoS ONE 11, e0167948. https://doi.org/10.1371/journal.pone.0167948 (2016).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    15.
    Walther, D., Scheuch, D. E. & Kampen, H. The invasive Asian tiger mosquito Aedes albopictus (Diptera: Culicidae) in Germany: Local reproduction and overwintering. Acta Trop. 166, 186–192 (2017).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    16.
    Werner, D. & Kampen, H. Aedes albopictus breeding in southern Germany, 2014. Parasitol. Res. 114, 831–834 (2015).
    PubMed  Article  PubMed Central  Google Scholar 

    17.
    Zielke, D. E., Walther, D. & Kampen, H. Newly discovered population of Aedes japonicus japonicus (Diptera: Culicidae) in upper Bavaria, Germany, and Salzburg, Austria, is closely related to the Austrian/Slovenian bush mosquito population. Parasit. Vectors 9, 163. https://doi.org/10.1186/s13071-016-1447-z (2016).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    18.
    Kampen, H., Jansen, S., Schmidt-Chanasit, J. & Walther, D. Indoor development of Aedes aegypti in Germany, 2016. Euro Surveill. 21, 30407. https://doi.org/10.2807/1560-7917.ES.2016.21.47.30407 (2016).
    Article  PubMed  PubMed Central  Google Scholar 

    19.
    Werner, D., Zielke, D. E. & Kampen, H. First record of Aedes koreicus (Diptera: Culicidae) in Germany. Parasitol. Res. 115, 1331–1334 (2016).
    PubMed  Article  Google Scholar 

    20.
    Kampen, H., Kronefeld, M., Zielke, D. & Werner, D. Three rarely encountered and one new Culiseta species (Diptera: Culicidae) in Germany. J. Eur. Mosq. Control Assoc. 31, 36–39 (2013).
    Google Scholar 

    21.
    Kampen, H., Kronefeld, M., Zielke, D. & Werner, D. Some new, rare and less frequent mosquito species (Diptera, Culicidae) recently collected in Germany. Mitt. Dtsch. Ges. Allg. Angew. Ent. 19, 123–130 (2014).
    Google Scholar 

    22.
    Isaac, N. J. B. et al. Statistics for citizen science: Extracting signals of change from noisy ecological data. Methods Ecol. Evol. 5, 1052–1060 (2014).
    Article  Google Scholar 

    23.
    Kuhlisch, C., Kampen, H. & Werner, D. On the distribution and ecology of Culiseta (Culicella) ochroptera (Peus) (Diptera: Culicidae) in Germany. Zootaxa 4576, 544–558 (2019).
    Article  Google Scholar 

    24.
    Heym, E. C., Schröder, J., Kampen, H. & Walther, D. The nuisance mosquito Anopheles plumbeus (Stephens, 1828) in Germany—A questionnaire survey may help support surveillance and control. Front. Public Health 5, 278. https://doi.org/10.3389/fpubh.2017.00278 (2017).
    Article  PubMed  PubMed Central  Google Scholar 

    25.
    Zielke, D. Population genetics and distribution of the invasive mosquito Aedes japonicus japonicus (Diptera: Culicidae) in Germany and Europe (Ph.D. thesis, University of Greifswald, 2015).

    26.
    Kerkow, A. et al. What makes the Asian bush mosquito Aedes japonicus japonicus feel comfortable in Germany? A fuzzy modelling approach. Parasit. Vectors 12, 106. https://doi.org/10.1186/s13071-019-3368-0 (2019).
    Article  PubMed  PubMed Central  Google Scholar 

    27.
    Boakes, E. H. et al. Patterns of contribution to citizen science biodiversity projects increase understanding of volunteers’ recording behaviour. Sci. Rep. 6, 33051. https://doi.org/10.1038/srep33051 (2016).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    28.
    Seymour, V. & Haklay, M. Exploring engagement characteristics and behaviours of environmental volunteers. Citiz. Sci. Theory Pract. 2, 5. https://doi.org/10.5334/cstp.66 (2017).
    Article  Google Scholar 

    29.
    Mair, L. & Ruete, A. Explaining spatial variation in the recording effort of citizen science data across multiple taxa. PLoS ONE 11, e0147796. https://doi.org/10.1371/journal.pone.0147796 (2016).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    30.
    Tiago, P., Ceia-Hasse, A., Marques, T. A., Capinha, C. & Pereira, H. M. Spatial distribution of citizen science casuistic observations for different taxonomic groups. Sci. Rep. 7, 12832. https://doi.org/10.1038/s41598-017-13130-8 (2017).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    31.
    Chandler, M. et al. Contributions to publications and management plans from 7 years of citizen science: Use of a novel evaluation tool on Earthwatch-supported projects. Biol. Conserv. 208, 163–173 (2017).
    Article  Google Scholar 

    32.
    Kelling, S. et al. Taking a “Big Data” approach to data quality in a citizen science project. Ambio 44, 601–611 (2015).
    PubMed  PubMed Central  Article  Google Scholar 

    33.
    Becker, N. et al. Mosquitoes and Their Control (Springer, Heidelberg, 2010).
    Google Scholar 

    34.
    Schaffner, F. et al. The Mosquitoes of Europe. An Identification and Training Programme (CD-Rom) (IRD Éditions & EID Méditerrannée, Montpellier, 2001).
    Google Scholar 

    35.
    Heym, E. C., Kampen, H. & Walther, D. Mosquito species composition and phenology (Diptera, Culicidae) in two German zoological gardens imply different risks of mosquito-borne pathogen transmission. J. Vector Ecol. 43, 80–88 (2018).
    PubMed  Article  PubMed Central  Google Scholar 

    36.
    European Union, Copernicus Land Monitoring Service. (European Environment Agency (EEA), 2012).

    37.
    Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, New York, 2016).
    Google Scholar 

    38.
    Tennekes, M. treemap: Treemap Visualization. R package version 2.4-2 (2017).

    39.
    Comtois, D. summarytools: Tools to Quickly and Neatly Summarize Data. R package version 0.9.3 (2019).

    40.
    R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, 2018).
    Google Scholar 

    41.
    Alender, B. Understanding volunteer motivations to participate in citizen science projects: A deeper look at water quality monitoring. J. Sci. Commun. 15, A04. https://doi.org/10.22323/2.15030204 (2016).
    Article  Google Scholar 

    42.
    Domroese, M. C. & Johnson, E. A. Why watch bees? Motivations of citizen science volunteers in the Great Pollinator Project. Biol. Conserv. 208, 40–47 (2017).
    Article  Google Scholar 

    43.
    Geoghegan, H., Dyke, A., Pateman, R., West, S. & Everett, G. Understanding Motivations for Citizen Science. Final report on behalf of UKEOF (University of Reading, Stockholm Environment Institute (University of York) and University of the West of England, 2016).

    44.
    Land-Zandstra, A. M., Devilee, J. L., Snik, F., Buurmeijer, F. & van den Broek, J. M. Citizen science on a smartphone: Participants’ motivations and learning. Public Underst. Sci. 25, 45–60 (2016).
    PubMed  Article  PubMed Central  Google Scholar 

    45.
    GeoBasis-DE/BKG. Bundesamt für Kartographie und Geodäsie. WFS service. http://sg.geodatenzentrum.de/wfs_dlm250_inspire?request=GetCapabilities&service=wfs (2019).

    46.
    Statistisches Bundesamt, Wiesbaden. https://ergebnisse.zensus2011.de/ (2015).

    47.
    Deutscher Wetterdienst (German Weather Service, single values averaged). https://opendata.dwd.de/climate_environment/ (2020).

    48.
    Pebesma, E. Simple Features for R: Standardized support for spatial vector data. R J. 10, 439–446. https://doi.org/10.32614/rj-2018-009 (2018).
    Article  Google Scholar 

    49.
    Cheng, J., Karambelkar, B. & Xie, Y. leaflet: Create Interactive Web Maps with the JavaScript ‘Leaflet’ Library. R package version 2.0.3 (2019).

    50.
    Hijmans, R. J. raster: Geographic Data Analysis and Modeling. R package version 2.8-19 (2019).

    51.
    Bivand, R., Keitt, T. & Rowlingson, B. rgdal: Bindings for the ‘Geospatial’ Data Abstraction Library. R package version 1.4-3 (2019).

    52.
    Baddeley, A., Rubak, E. & Turner, R. Spatial Point Patterns: Methodology and Applications with R (Chapman and Hall/CRC Press, Boca Raton, 2015).
    Google Scholar 

    53.
    Fox, J. & Weisberg, S. An R Companion to Applied Regression (Sage, Thousand Oaks, 2019).
    Google Scholar 

    54.
    Kleiber, C. & Zeileis, A. countreg: Count Data Regression. R package version 0.2-1 (2016).

    55.
    Barton, K. MuMIn: Multi-model Inference. R package version 1.43.6 (2019).

    56.
    Venables, W. N. & Ripley, B. D. Modern Applied Statistics with S (Springer, New York, 2002).
    Google Scholar 

    57.
    Zeileis, A., Kleiber, C. & Jackman, S. Regression models for count data in R. J. Stat. Softw. https://doi.org/10.18637/jss.v027.i08 (2008).
    Article  Google Scholar 

    58.
    Bertone, M. A. et al. Arthropods of the great indoors: Characterizing diversity inside urban and suburban homes. PeerJ 4, e1582. https://doi.org/10.7717/peerj.1582 (2016).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    59.
    Epps, M. J., Menninger, H. L., LaSala, N. & Dunn, R. R. Too big to be noticed: Cryptic invasion of Asian camel crickets in North American houses. PeerJ 2, e523. https://doi.org/10.7717/peerj.523 (2014).
    Article  PubMed  PubMed Central  Google Scholar 

    60.
    Dunn, R. R. & Beasley, D. E. Democratizing evolutionary biology, lessons from insects. Curr. Opin. Insect Sci. 18, 89–92 (2016).
    PubMed  Article  PubMed Central  Google Scholar 

    61.
    Hamer, S. A., Curtis-Robles, R. & Hamer, G. L. Contributions of citizen scientists to arthropod vector data in the age of digital epidemiology. Curr. Opin. Insect Sci. 28, 98–104 (2018).
    PubMed  Article  PubMed Central  Google Scholar 

    62.
    Freitag, H., Pangantihon, C. V. & Njunjic, I. Three new species of Grouvellinus Champion, 1923 from Maliau Basin, Sabah, Borneo, discovered by citizen scientists during the first Taxon Expedition (Insecta, Coleoptera, Elmidae). ZooKeys 754, 1–21 (2018).
    Article  Google Scholar 

    63.
    Higa, M. et al. Mapping large-scale bird distributions using occupancy models and citizen data with spatially biased sampling effort. Divers. Distrib. 21, 46–54 (2015).
    Article  Google Scholar 

    64.
    Caputo, B. et al. ZanzaMapp: A scalable citizen science tool to monitor perception of mosquito abundance and nuisance in Italy and beyond. Int. J. Environ. Res. Public Health 17, 7872 (2020).
    PubMed Central  Article  Google Scholar 

    65.
    Curtis-Robles, R., Wozniak, E. J., Auckland, L. D., Hamer, G. L. & Hamer, S. A. Combining public health education and disease ecology research: Using citizen science to assess Chagas disease entomological risk in Texas. PLoS Negl. Trop. Dis. 9, e0004235. https://doi.org/10.1371/journal.pntd.0004235 (2015).
    Article  PubMed  PubMed Central  Google Scholar 

    66.
    Soroye, P., Ahmed, N. & Kerr, J. T. Opportunistic citizen science data transform understanding of species distributions, phenology, and diversity gradients for global change research. Glob. Change Biol. 24, 5281–5291 (2018).
    ADS  Article  Google Scholar 

    67.
    Statistisches Bundesamt. Bevölkerungsdichte (Einwohner je km2) in Deutschland nach Bundesländern zum 31. Dezember 2019 (Statista GmbH, 2020).

    68.
    Newman, G. et al. Leveraging the power of place in citizen science for effective conservation decision making. Biol. Conserv. 208, 55–64 (2017).
    Article  Google Scholar 

    69.
    Becker, N. Microbial control of mosquitoes: Management of the upper Rhine mosquito population as a model programme. Parasitol. Today 13, 485–487 (1997).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    70.
    Peus, F. Beiträge zur Faunistik und Ökologie der einheimischen Culiciden. I. Teil. Zeitschr. Desinfekt. 21(76–81), 92–98 (1929).
    Google Scholar 

    71.
    Vezzani, D. Artificial container-breeding mosquitoes and cemeteries: A perfect match. Trop. Med. Int. Health 12, 299–313 (2007).
    PubMed  Article  Google Scholar 

    72.
    Scharnweber, T. et al. Drought matters—declining precipitation influences growth of Fagus sylvatica L. and Quercus robur L. in north-eastern Germany. Forest Ecol. Manag. 262, 947–961 (2011).
    Article  Google Scholar 

    73.
    Oedekoven, C. S. et al. Attributing changes in the distribution of species abundance to weather variables using the example of British breeding birds. Methods Ecol. Evol. 8, 1690–1702 (2017).
    Article  Google Scholar 

    74.
    Catlin-Groves, C. L. The citizen science landscape: From volunteers to citizen sensors and beyond. Int. J. Zool. 2012, 349630 (2012).
    Article  Google Scholar 

    75.
    Kelling, S. et al. Using semistructured surveys to improve citizen science data for monitoring biodiversity. Bioscience 69, 170–179 (2019).
    PubMed  PubMed Central  Article  Google Scholar 

    76.
    Weiser, E. L. et al. Balancing sampling intensity against spatial coverage for a community science monitoring programme. J. Appl. Ecol. 56, 2252–2263 (2019).
    Article  Google Scholar 

    77.
    Mwangungulu, S. P. et al. Crowdsourcing vector surveillance: Using community knowledge and experiences to predict densities and distribution of outdoor-biting mosquitoes in rural Tanzania. PLoS ONE 11, e0156388. https://doi.org/10.1371/journal.pone.0156388 (2016).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    78.
    Eritja, R. et al. First detection of Aedes japonicus in Spain: An unexpected finding triggered by citizen science. Parasit. Vectors 12, 53. https://doi.org/10.1186/s13071-019-3317-y (2019).
    Article  PubMed  PubMed Central  Google Scholar  More

  • in

    Annual phytoplankton dynamics in coastal waters from Fildes Bay, Western Antarctic Peninsula

    1.
    Smetacek, V. & Nicol, S. Polar ocean ecosystems in a changing world. Nature 437, 362–368. https://doi.org/10.1038/nature04161 (2005).
    ADS  CAS  PubMed  Article  Google Scholar 
    2.
    Browning, T. J. et al. Nutrient regimes control phytoplankton ecophysiology in the South Atlantic. Biogeosciences 11, 463–479. https://doi.org/10.5194/bg-11-463-2014 (2014).
    ADS  Article  Google Scholar 

    3.
    Garibotti, I. A., Vernet, M. & Ferrario, M. E. Annually recurrent phytoplanktonic assemblages during summer in the seasonal ice zone west of the Antarctic Peninsula (Southern Ocean). Deep-Sea Res. Part I Oceanogr. Res. Pap. 52, 1823–1841. https://doi.org/10.1016/j.dsr.2005.05.003 (2005).
    ADS  Article  Google Scholar 

    4.
    Clem, K. R. et al. Record warming at the South Pole during the past three decades. Nat. Clim. Change 10, 762–770. https://doi.org/10.1038/s41558-020-0815-z (2020).
    ADS  Article  Google Scholar 

    5.
    Martinson, D. G., Stammerjohn, S. E., Iannuzzi, R. A., Smith, R. C. & Vernet, M. Western Antarctic Peninsula physical oceanography and spatio-temporal variability. Deep-Sea Res. Part II Top. Stud. Oceanogr. 55, 1964–1987. https://doi.org/10.1016/j.dsr2.2008.04.038 (2008).
    ADS  Article  Google Scholar 

    6.
    Schofield, O. et al. Changes in the upper ocean mixed layer and phytoplankton productivity along the West Antarctic Peninsula. Philos. Trans. R. Soc. A Math. Phys. Eng. Sci. 376, 20170173. https://doi.org/10.1098/rsta.2017.0173 (2018).
    ADS  CAS  Article  Google Scholar 

    7.
    Kim, H. et al. Inter-decadal variability of phytoplankton biomass along the coastal West Antarctic Peninsula. Philos. Trans. R. Soc. A Math. Phys. Eng. Sci. 376, 20170174. https://doi.org/10.1098/rsta.2017.0174 (2018).
    ADS  Article  Google Scholar 

    8.
    Lange, P. K., Ligowski, R. & Tenenbaum, D. R. Phytoplankton in the embayments of King George Island (Antarctic Peninsula): a review with emphasis on diatoms. Polar Rec. 54, 158–175. https://doi.org/10.1017/S0032247418000232 (2018).
    Article  Google Scholar 

    9.
    Kopczynska, E. Phytoplankton variability in Admiralty Bay, King George Island, South Shetland Islands: six years of monitoring. Pol. Polar Res. 29, 117–139 (2008).
    Google Scholar 

    10.
    Biggs, T. E. et al. Antarctic phytoplankton community composition and size structure: importance of ice type and temperature as regulatory factors. Polar Biol. 42, 1997–2015. https://doi.org/10.1007/s00300-019-02576-3 (2019).
    Article  Google Scholar 

    11.
    Assmy, P. et al. Leads in Arctic pack ice enable early phytoplankton blooms below snow-covered sea ice. Sci. Rep. 7, 1–9. https://doi.org/10.1038/srep40850 (2017).
    CAS  Article  Google Scholar 

    12.
    Egas, C. et al. Short timescale dynamics of phytoplankton in Fildes Bay, Antarctica. Antarct. Sci. 29, 217. https://doi.org/10.1017/S0954102016000699 (2017).
    ADS  Article  Google Scholar 

    13.
    Delmont, T. O., Hammar, K. M., Ducklow, H. W., Yager, P. L. & Post, A. F. Phaeocystis antarctica blooms strongly influence bacterial community structures in the Amundsen Sea polynya. Front. Microbiol. 5, 1–13. https://doi.org/10.3389/fmicb.2014.00646 (2014).
    Article  Google Scholar 

    14.
    Arrigo, K. R. et al. Phytoplankton community structure and the drawdown of nutrients and ({{rm CO}}_{2}) in the Southern Ocean. Science 283, 365–367. https://doi.org/10.1126/science.283.5400.365 (1999).
    ADS  CAS  PubMed  Google Scholar 

    15.
    Lin, Y. et al. Specific eukaryotic plankton are good predictors of net community production in the Western Antarctic Peninsula. Sci. Rep. 7, 1–11. https://doi.org/10.1038/s41598-017-14109-1 (2017).
    ADS  CAS  Article  Google Scholar 

    16.
    Alcamán-Arias, M. E., Farías, L., Verdugo, J., Alarcón-Schumacher, T. & Díez, B. Microbial activity during a coastal phytoplankton bloom on the Western Antarctic Peninsula in late summer. FEMS Microbiol. Lett. 365, 1–13. https://doi.org/10.1093/femsle/fny090 (2018).
    CAS  Article  Google Scholar 

    17.
    Moreno-Pino, M. et al. Variation in coastal Antarctic microbial community composition at sub-mesoscale: spatial distance or environmental filtering? FEMS Microbiol. Ecol. 92, fiw088. https://doi.org/10.1093/femsec/fiw088 (2016).
    CAS  PubMed  Article  Google Scholar 

    18.
    Moon-van der Staay, S. Y., De Wachter, R. & Vaulot, D. Oceanic 18S rDNA sequences from picoplankton reveal unsuspected eukaryotic diversity. Nature 409, 607–610. https://doi.org/10.1038/35054541 (2001).
    ADS  CAS  PubMed  Article  Google Scholar 

    19.
    Fuller, N. J. et al. Analysis of photosynthetic picoeukaryote diversity at open ocean sites in the Arabian Sea using a PCR biased towards marine algal plastids. Aquat. Microbial Ecol. 43, 79–93 (2006).
    Article  Google Scholar 

    20.
    Shi, X. L., Lepère, C., Scanlan, D. J. & Vaulot, D. Plastid 16S rRNA gene diversity among eukaryotic picophytoplankton sorted by flow cytometry from the South Pacific Ocean. PLoS ONE 6, e18979 (2011).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    21.
    Sieburth, J. M., Smetacek, V. & Lenz, J. Pelagic ecosystem structure: heterotrophic compartments of the plankton and their relationship to plankton size fractions. Limnol. Oceanogr. 23, 1256–1263 (1978).
    ADS  Article  Google Scholar 

    22.
    Marie, D., Shi, X. L., Rigaut-Jalabert, F. & Vaulot, D. Use of flow cytometric sorting to better assess the diversity of small photosynthetic eukaryotes in the English Channel. FEMS Microbiol. Ecol. 72, 165–178 (2010).
    CAS  PubMed  Article  Google Scholar 

    23.
    Balzano, S., Marie, D., Gourvil, P. & Vaulot, D. Composition of the summer photosynthetic pico and nanoplankton communities in the Beaufort Sea assessed by T-RFLP and sequences of the 18S rRNA gene from flow cytometry sorted samples. ISME J. 6, 1480–1498. https://doi.org/10.1038/ismej.2011.213 (2012).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    24.
    Callahan, B. J. et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583. https://doi.org/10.1038/nmeth.3869 (2016).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    25.
    Jeong, H. J. et al. Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean Sci. J. 45, 65–91. https://doi.org/10.1007/s12601-010-0007-2 (2010).
    ADS  CAS  Article  Google Scholar 

    26.
    Wilks, J. V. & Armand, L. K. Diversity and taxonomic identification of Shionodiscus spp. in the Australian sector of the Subantarctic Zone. Diatom Res. 32, 295–307. https://doi.org/10.1080/0269249X.2017.1365015 (2017).
    Article  Google Scholar 

    27.
    Moreno, C. M. et al. Examination of gene repertoires and physiological responses to iron and light limitation in Southern Ocean diatoms. Polar Biol. 41, 679–696. https://doi.org/10.1007/s00300-017-2228-7 (2018).
    Article  Google Scholar 

    28.
    Balzano, S. et al. Morphological and genetic diversity of Beaufort Sea diatoms with high contributions from the Chaetoceros neogracilis species complex. J. Phycol. 53, 161–187. https://doi.org/10.1111/jpy.12489 (2017).
    CAS  PubMed  Article  Google Scholar 

    29.
    Worden, A. Z. et al. Global distribution of a wild alga revealed by targeted metagenomics. Curr. Biol. 22, R675–R677 (2012).
    CAS  PubMed  Article  Google Scholar 

    30.
    Balzano, S. et al. Diversity of cultured photosynthetic flagellates in the North East Pacific and Arctic Oceans in summer. Biogeosciences 9, 4553–4571. https://doi.org/10.5194/bg-9-4553-2012 (2012).
    ADS  CAS  Article  Google Scholar 

    31.
    Kuwata, A. et al. Bolidophyceae, a sister picoplanktonic group of diatoms—a review. Front. Mar. Sci. 5, 370. https://doi.org/10.3389/fmars.2018.00370 (2018).
    Article  Google Scholar 

    32.
    Massana, R., del Campo, J., Sieracki, M. E., Audic, S. & Logares, R. Exploring the uncultured microeukaryote majority in the oceans: reevaluation of ribogroups within stramenopiles. ISME J. 8, 854–866 (2014).
    PubMed  Article  Google Scholar 

    33.
    Tragin, M. & Vaulot, D. Novel diversity within marine Mamiellophyceae (Chlorophyta) unveiled by metabarcoding. Sci. Rep. 9, 5190. https://doi.org/10.1038/s41598-019-41680-6 (2019).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    34.
    van den Hoff, J., Bell, E. & Whittock, L. Dimorphism in the Antarctic cryptophyte Geminigera cryophila (Cryptophyceae). J. Phycol. 56, 1028–1038. https://doi.org/10.1111/jpy.13004 (2020).
    CAS  PubMed  Article  Google Scholar 

    35.
    Needham, D. M. & Fuhrman, J. A. Pronounced daily succession of phytoplankton, archaea and bacteria following a spring bloom. Nat. Microbiol. 1, 16005. https://doi.org/10.1038/nmicrobiol.2016.5 (2016).
    CAS  PubMed  Article  Google Scholar 

    36.
    Lin, Y., Gifford, S., Ducklow, H., Schofield, O. & Cassar, N. Towards quantitative microbiome community profiling using internal standards. Appl. Environ. Microbiol. 85, 1–14 (2019).
    Google Scholar 

    37.
    van Leeuwe, M. A. et al. Annual patterns in phytoplankton phenology in Antarctic coastal waters explained by environmental drivers. Limnol. Oceanogr. 65, 1651–1668. https://doi.org/10.1002/lno.11477 (2020).
    ADS  Article  Google Scholar 

    38.
    Wasilowska, A., Kopczynska, E. E. & Rzepecki, M. Temporal and spatial variation of phytoplankton in Admiralty Bay, South Shetlands: the dynamics of summer blooms shown by pigment and light microscopy analysis. Polar Biol. 38, 1249–1265. https://doi.org/10.1007/s00300-015-1691-2 (2015).
    Article  Google Scholar 

    39.
    Rozema, P. D. et al. Summer microbial community composition governed by upper-ocean stratification and nutrient availability in northern Marguerite Bay, Antarctica. Deep Sea Res. Part II Top. Stud. Oceanogr. 139, 151–166. https://doi.org/10.1016/j.dsr2.2016.11.016 (2016).
    ADS  CAS  Article  Google Scholar 

    40.
    Annett, A. L., Carson, D. S., Crosta, X., Clarke, A. & Ganeshram, R. S. Seasonal progression of diatom assemblages in surface waters of Ryder Bay, Antarctica. Polar Biol. 33, 13–29. https://doi.org/10.1007/s00300-009-0681-7 (2010).
    Article  Google Scholar 

    41.
    Garibotti, I. et al. Phytoplankton spatial distribution patterns along the western Antarctic Peninsula (Southern Ocean). Mar. Ecol. Prog. Ser. 261, 21–39. https://doi.org/10.3354/meps261021 (2003).
    ADS  Article  Google Scholar 

    42.
    de Lima, D. T. et al. Abiotic changes driving microphytoplankton functional diversity in Admiralty Bay, King George Island (Antarctica). Front. Mar. Sci. 6, 1–17. https://doi.org/10.3389/fmars.2019.00638 (2019).
    ADS  CAS  Article  Google Scholar 

    43.
    Luria, C. M., Ducklow, H. W. & Amaral-Zettler, L. A. Marine bacterial, archaeal and eukaryotic diversity and community structure on the continental shelf of the western Antarctic Peninsula. Aquat. Microbial Ecol. 73, 107–121. https://doi.org/10.3354/ame01703 (2014).
    Article  Google Scholar 

    44.
    Luo, W. et al. Molecular diversity of microbial eukaryotes in sea water from Fildes Peninsula, King George Island, Antarctica. Polar Biol. 39, 605–616. https://doi.org/10.1007/s00300-015-1815-8 (2016).
    ADS  Article  Google Scholar 

    45.
    Rozema, P. D. et al. Interannual variability in phytoplankton biomass and species composition in northern Marguerite Bay (West Antarctic Peninsula) is governed by both winter sea ice cover and summer stratification. Limnol. Oceanogr. 62, 235–252. https://doi.org/10.1002/lno.10391 (2017).
    ADS  Article  Google Scholar 

    46.
    Lee, S. H. et al. Large contribution of small phytoplankton at Marian Cove, King George Island, Antarctica, based on long-term monitoring from 1996 to 2008. Polar Biol. 38, 207–220. https://doi.org/10.1007/s00300-014-1579-6 (2015).
    Article  Google Scholar 

    47.
    Kang, J. S., Kang, S. H., Kim, D. & Kim, D. Y. Planktonic centric diatom Minidiscus chilensis dominated sediment trap material in eastern Bransfield Strait, Antarctica. Mar. Ecol. Prog. Ser. 255, 93–99 (2003).
    ADS  Article  Google Scholar 

    48.
    Vaulot, D., Eikrem, W., Viprey, M. & Moreau, H. The diversity of small eukaryotic phytoplankton ((le 3 upmu {{rm m}})) in marine ecosystems. FEMS Microbiol. Rev. 32, 795–820. https://doi.org/10.1111/j.1574-6976.2008.00121.x (2008).
    CAS  PubMed  Google Scholar 

    49.
    Andersen, R. A., Saunders, G. W., Paskind, M. P. & Sexton, J. Ultrastructure and 18S rRNA gene sequence for Pelagomonas calceolata gen. and sp. nov. and the description of a new algal class, the Pelagophyceae classis nov. J. Phycol. 29, 701–715 (1993).
    CAS  Article  Google Scholar 

    50.
    Dìez, B., Pedrós-Alió, C. & Massana, R. Study of genetic diversity of eukaryotic picoplankton in different oceanic regions by small-subunit rRNA gene cloning and sequencing. Appl. Environ. Microbiol. 67, 2932–2941. https://doi.org/10.1128/AEM.67.7.2932-2941.2001 (2001).
    PubMed  PubMed Central  Article  Google Scholar 

    51.
    Gérikas Ribeiro, C. et al. Culturable diversity of Arctic phytoplankton during pack ice melting. Elem. Sci. Anthropocene 8, 6. https://doi.org/10.1525/elementa.401 (2020).
    Article  Google Scholar 

    52.
    Sow, L. S. S., Trull, T. W. & Bodrossy, L. Oceanographic fronts shape Phaeocystis assemblages: a high-resolution 18S rRNA gene survey from the ice-edge to the equator of the South Pacific. Front. Microbiol. 11, 1847. https://doi.org/10.3389/fmicb.2020.01847 (2020).
    PubMed  PubMed Central  Article  Google Scholar 

    53.
    Gaebler, S., Hayes, P. K. & Medlin, L. K. Methods used to reveal genetic diversity in the colony-forming prymnesiophytes Phaeocystis antarctica, P. globosa and P. pouchetii—preliminary results. In Phaeocystis Major Link in the Biogeochemical Cycling of Climate-Relevant Elements (eds van Leeuwe, M. et al.) 330 (Springer Netherlands, Houten, 2007). https://doi.org/10.1007/978-1-4020-6214-8.
    Google Scholar 

    54.
    DiTullio, G. R. et al. Rapid and early export of Phaeocystis antarctica blooms in the Ross Sea, Antarctica. Nature 404, 595–598. https://doi.org/10.1038/35007061 (2000).
    ADS  CAS  PubMed  Article  Google Scholar 

    55.
    Arrigo, K. R. et al. Phytoplankton taxonomic variability in nutrient utilization and primary production in the Ross Sea. J. Geophys. Res. Oceans 105, 8827–8846. https://doi.org/10.1029/1998JC000289 (2000).
    ADS  CAS  Article  Google Scholar 

    56.
    van Leeuwe, M. A. & Stefels, J. Photosynthetic responses in Phaeocystis antarctica towards varying light and iron conditions. Biogeochemistry 83, 61–70. https://doi.org/10.1007/s10533-007-9083-5 (2007).
    CAS  Article  Google Scholar 

    57.
    Gast, R. J., McKie-Krisberg, Z. M., Fay, S. A., Rose, J. M. & Sanders, R. W. Antarctic mixotrophic protist abundances by microscopy and molecular methods. FEMS Microbiol. Ecol. 89, 388–401. https://doi.org/10.1111/1574-6941.12334 (2014).
    CAS  PubMed  Article  Google Scholar 

    58.
    Sekiguchi, H., Kawachi, M., Nakayama, T. & Inouye, I. A taxonomic re-evaluation of the Pedinellales (Dictyochophyceae), based on morphological, behavioural and molecular data. Phycologia 42, 165–182. https://doi.org/10.2216/i0031-8884-42-2-165.1 (2003).
    Article  Google Scholar 

    59.
    Li, Q., Edwards, K. F., Schvarcz, C. R., Selph, K. E. & Steward, G. F. Plasticity in the grazing ecophysiology of Florenciella (Dichtyochophyceae), a mixotrophic nanoflagellate that consumes Prochlorococcus and other bacteria. Limnol. Oceanogr.. https://doi.org/10.1002/lno.11585 (2020).
    CAS  Article  Google Scholar 

    60.
    Maruyama, S. & Kim, E. A modern descendant of early green algal phagotrophs. Curr. Biol. 23, 1081–1084. https://doi.org/10.1016/j.cub.2013.04.063 (2013).
    CAS  PubMed  Article  Google Scholar 

    61.
    Darling, K. F. et al. Molecular evidence for genetic mixing of Arctic and Antarctic subpolar populations of planktonic foraminifers. Nature 405, 43–47. https://doi.org/10.1038/35011002 (2000).
    ADS  CAS  PubMed  Article  Google Scholar 

    62.
    Sul, W. J., Oliver, T. A., Ducklow, H. W., Amaral-Zettler, L. A. & Sogin, M. L. Marine bacteria exhibit a bipolar distribution. Proc. Natl. Acad. Sci. USA 110, 2342–2347. https://doi.org/10.1073/pnas.1212424110 (2013).
    ADS  PubMed  Article  Google Scholar 

    63.
    Wolf, C., Kilias, E. & Metfies, K. Protists in the polar regions: comparing occurrence in the Arctic and Southern oceans using pyrosequencing. Polar Res. 34, 23225. https://doi.org/10.3402/polar.v34.23225 (2015).
    Article  Google Scholar 

    64.
    Lovejoy, C. & Potvin, M. Microbial eukaryotic distribution in a dynamic Beaufort Sea and the Arctic Ocean. J. Plankton Res. 33, 431–444. https://doi.org/10.1093/plankt/fbq124 (2011).
    Article  Google Scholar 

    65.
    Delmont, T. O., Murat Eren, A., Vineis, J. H. & Post, A. F. Genome reconstructions indicate the partitioning of ecological functions inside a phytoplankton bloom in the Amundsen Sea, Antarctica. Front. Microbiol. 6, 1–19. https://doi.org/10.3389/fmicb.2015.01090 (2015).
    Article  Google Scholar 

    66.
    Simmons, M. P. et al. Intron invasions trace algal speciation and reveal nearly identical arctic and antarctic Micromonas populations. Mol. Biol. Evol. 32, 2219–2235. https://doi.org/10.1093/molbev/msv122 (2015).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    67.
    Joli, N., Monier, A., Logares, R. & Lovejoy, C. Seasonal patterns in Arctic prasinophytes and inferred ecology of Bathycoccus unveiled in an Arctic winter metagenome. ISME J. 6, 1372–1385. https://doi.org/10.1038/ismej.2017.7 (2017).
    Article  Google Scholar 

    68.
    Benner, I., Irwin, A. J. & Finkel, Z. Capacity of the common Arctic picoeukaryote Micromonas to adapt to a warming warming ocean. Limnol. Oceanogr. Lett. 5, 221–227 (2019).
    Article  Google Scholar 

    69.
    Li, W. K., McLaughlin, F. A., Lovejoy, C. & Carmack, E. C. Smallest algae thrive as the Arctic Ocean freshens. Science 326, 539. https://doi.org/10.1126/science.1179798 (2009).
    ADS  CAS  PubMed  Article  Google Scholar 

    70.
    Hoppe, C. J. M., Flintrop, C. M. & Rost, B. The arctic picoeukaryote Micromonas pusilla benefits synergistically from warming and ocean acidification. Biogeosciences 15, 4353–4365. https://doi.org/10.5194/bg-15-4353-2018 (2018).
    ADS  CAS  Article  Google Scholar 

    71.
    Vannier, T. et al. Survey of the green picoalga Bathycoccus genomes in the global ocean. Sci. Rep. 6, 37900. https://doi.org/10.1038/srep37900 (2016).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    72.
    Vaulot, D. et al. Metagenomes of the Picoalga Bathycoccus from the Chile coastal upwelling. PLoS ONE 7, e39648. https://doi.org/10.1371/journal.pone.0039648 (2012).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    73.
    Kauko, H. M. et al. Algal colonization of young Arctic sea ice in spring. Front. Mar. Sci. 5, 1–20. https://doi.org/10.3389/fmars.2018.00199 (2018).
    Article  Google Scholar 

    74.
    Schloss, I. R. et al. On the phytoplankton bloom in coastal waters of southern King George Island (Antarctica) in January 2010: an exceptional feature? Limnol. Oceanogr. 59, 195–210. https://doi.org/10.4319/lo.2014.59.1.0195 (2014).
    ADS  CAS  Article  Google Scholar 

    75.
    Świło, M., Majewski, W., Minzoni, R. T. & Anderson, J. B. Diatom assemblages from coastal settings of West Antarctica. Mar. Micropaleontol. 125, 95–109. https://doi.org/10.1016/j.marmicro.2016.04.001 (2016).
    ADS  Article  Google Scholar 

    76.
    Pike, J. et al. Observations on the relationship between the Antarctic coastal diatoms Thalassiosira antarctica Comber and Porosira glacialis (Grunow) Jørgensen and sea ice concentrations during the late Quaternary. Mar. Micropaleontol. 73, 14–25. https://doi.org/10.1016/j.marmicro.2009.06.005 (2009).
    ADS  Article  Google Scholar 

    77.
    Luddington, I. A., Lovejoy, C. & Kaczmarska, I. Species-rich meta-communities of the diatom order Thalassiosirales in the Arctic and northern Atlantic Ocean. J. Plankton Res. 38, 781–797. https://doi.org/10.1093/plankt/fbw030 (2016).
    CAS  Article  Google Scholar 

    78.
    Hoppenrath, M. et al. Thalassiosira species (Bacillariophyceae, Thalassiosirales) in the North Sea at Helgoland (German Bight) and Sylt (North Frisian Wadden Sea) – A first approach to assessing diversity. Eur. J. Phycol. 42, 271–288. https://doi.org/10.1080/09670260701352288 (2007).
    Article  Google Scholar 

    79.
    Schoemann, V., Becquevort, S., Stefels, J., Rousseau, V. & Lancelot, C. Phaeocystis blooms in the global ocean and their controlling mechanisms: a review. J. Sea Res. 53, 43–66. https://doi.org/10.1016/j.seares.2004.01.008 (2005).
    ADS  CAS  Article  Google Scholar 

    80.
    Lange, M., Chen, Y. Q. & Medlin, L. K. Molecular genetic delineation of Phaeocystis species (Prymnesiophyceae) using coding and non-coding regions of nuclear and plastid genomes. Eur. J. Phycol. 37, 77–92. https://doi.org/10.1017/S0967026201003481 (2002).
    Article  Google Scholar 

    81.
    Medlin, L. K., Lange, M. & Baumann, M. E. Genetic differentiation among three colony-forming species of Phaeocystis: further evidence for the phylogeny of the Prymnesiophyta. Phycologia 33, 199–212. https://doi.org/10.2216/i0031-8884-33-3-199.1 (1994).
    Article  Google Scholar 

    82.
    Thompson, D. W. & Solomon, S. Interpretation of recent Southern Hemisphere climate change. Science 296, 895–899. https://doi.org/10.1126/science.1069270 (2002).
    ADS  CAS  PubMed  Article  Google Scholar 

    83.
    Smith, R. C. & Stammerjohn, S. E. Variations of surface air temperature and sea-ice extent in the western Antarctic Peninsula region. Ann. Glaciol. 33, 493–500. https://doi.org/10.3189/172756401781818662 (2001).
    ADS  Article  Google Scholar 

    84.
    Hansen, M. O., Nielsen, T. G., Stedmon, C. A. & Munk, P. Oceanographic regime shift during 1997 in Disko Bay, Western Greenland. Limnol. Oceanogr. 57, 634–644. https://doi.org/10.4319/lo.2012.57.2.0634 (2012).
    ADS  Article  Google Scholar 

    85.
    Holm-Hansen, O., Lorenzen, C. J., Holmes, R. W. & Strickland, J. D. H. Fluorometric determination of chlorophyll. ICES J. Mar. Sci. 30, 3–15. https://doi.org/10.1093/icesjms/30.1.3 (1965).
    CAS  Article  Google Scholar 

    86.
    Marie, D., Rigaut-Jalabert, F. & Vaulot, D. An improved protocol for flow cytometry analysis of phytoplankton cultures and natural samples. Cytometry 85, 962–968. https://doi.org/10.1002/cyto.a.22517 (2014).
    CAS  PubMed  Article  Google Scholar 

    87.
    Gérikas Ribeiro, C., Lopes dos Santos, A., Marie, D., Pereira Brandini, F. & Vaulot, D. Small eukaryotic phytoplankton communities in tropical waters off Brazil are dominated by symbioses between Haptophyta and nitrogen-fixing cyanobacteria. ISME J. 12, 1360–1374. https://doi.org/10.1038/s41396-018-0050-z (2018).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    88.
    Piredda, R. et al. Diversity and temporal patterns of planktonic protist assemblages at a Mediterranean Long Term Ecological Research site. FEMS Microbiol. Ecol. 93, fiw200. https://doi.org/10.1093/femsec/fiw200 (2017).
    CAS  PubMed  Article  Google Scholar 

    89.
    Lepère, C. et al. Whole Genome Amplification (WGA) of marine photosynthetic eukaryote populations. FEMS Microbiol. Ecol. 76, 516–523 (2011).
    Article  Google Scholar 

    90.
    Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 17, 10–12. https://doi.org/10.14806/ej.17.1.200 (2011).
    Article  Google Scholar 

    91.
    R Development Core Team. R: A Language and Environment for Statistical Computing. https://doi.org/10.1007/978-3-540-74686-7 (2013).

    92.
    Guillou, L. et al. The Protist Ribosomal Reference database (({{rm PR}}^{2})): a catalog of unicellular eukaryote Small Sub-Unit rRNA sequences with curated taxonomy. Nucleic Acids Res. 41, D597–D604. https://doi.org/10.1093/nar/gks1160 (2013).
    CAS  PubMed  Google Scholar 

    93.
    Decelle, J. et al. PhytoREF: a reference database of the plastidial 16S rRNA gene of photosynthetic eukaryotes with curated taxonomy. Mol. Ecol. Resour. 15, 1435–1445. https://doi.org/10.1111/1755-0998.12401 (2015).
    CAS  PubMed  Article  Google Scholar 

    94.
    Wickham, H., François, R., Henry, L. & Müller, K. dplyr: A Grammar of Data Manipulation. R package version 1.0.2. (2020)

    95.
    Wilkins, D. treemapify: Draw Treemaps in ’ggplot2’. R package version 2.5.3. (2019)

    96.
    McMurdie, P. J. & Holmes, S. phyloseq: an r package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8, 1–11. https://doi.org/10.1371/journal.pone.0061217 (2013).
    CAS  Article  Google Scholar 

    97.
    Dixon, P. Vegan, a package of r functions for community ecology. J. Veg. Sci. 14, 927–930. https://doi.org/10.1111/j.1654-1103.2003.tb02228.x (2003).
    Article  Google Scholar 

    98.
    Gehlenborg, N. UpSetR: A More Scalable Alternative to Venn and Euler Diagrams for Visualizing Intersecting Sets. R package version 1.4.0. (2019) More

  • in

    Preference, performance, and chemical defense in an endangered butterfly using novel and ancestral host plants

    1.
    Strauss, S. Y., Lau, J. A. & Carroll, S. P. Evolutionary responses of natives to introduced species: what do introductions tell us about natural communities? Evolutionary responses of natives to introduced species. Ecol. Lett. 9, 357–374 (2006).
    PubMed  Article  Google Scholar 
    2.
    Smith, D. C. Heritable divergence of Rhagoletis pomonella host races by seasonal asynchrony. Nature 336, 66–67 (1988).
    ADS  Article  Google Scholar 

    3.
    Filchak, K. E., Roethele, J. B. & Feder, J. L. Natural selection and sympatric divergence in the apple maggot Rhagoletis pomonella. Nature 407, 739–742 (2000).
    ADS  CAS  PubMed  Article  Google Scholar 

    4.
    Carroll, S. P., Dingle, H., Famula, T. R. & Fox, C. W. Genetic architecture of adaptive differentiation in evolving host races of the soapberry bug, Jadera haematoloma. in Microevolution Rate, Pattern, Process (eds. Hendry, A. P. & Kinnison, M. T.) vol. 8 257–272 (Springer Netherlands, 2001).

    5.
    Nice, C. C., Fordyce, J. A., Shapiro, A. M. & Ffrench-Constant, R. Lack of evidence for reproductive isolation among ecologically specialised lycaenid butterflies. Ecol. Entomol. 27, 702–712 (2002).
    Article  Google Scholar 

    6.
    Graves, S. D. & Shapiro, A. M. Exotics as host plants of the California butterfly fauna. 110, 413–433 (2003).
    Google Scholar 

    7.
    Thomas, J. A., Simcox, D. J. & Hovestadt, T. Evidence based conservation of butterflies. J. Insect Conserv. 15, 241–258 (2011).
    Article  Google Scholar 

    8.
    Battin, J. When good animals love bad habitats: Ecological traps and the conservation of animal populations. Conserv. Biol. 18, 1482–1491 (2004).
    Article  Google Scholar 

    9.
    Casagrande, R.A. & Dacey, J. E. Monarch butterfly oviposition on swallow-worts (Vincetoxicum spp.). Environ. Entomol. 36, 631–636 (2007).

    10.
    Davis, S. L. & Cipollini, D. Do mothers always know best? Oviposition mistakes and resulting larval failure of Pieris virginiensis on Alliaria petiolata, a novel, toxic host. Biol. Invasions 16, 1941–1950 (2014).
    Article  Google Scholar 

    11.
    Janzen, D. H. On ecological fitting. Oikos 45, 308 (1985).
    Article  Google Scholar 

    12.
    Singer, M. C. & Parmesan, C. Lethal trap created by adaptive evolutionary response to an exotic resource. Nature 557, 238–241 (2018).
    ADS  CAS  PubMed  Article  Google Scholar 

    13.
    Thomas, C. D. et al. Incorporation of a European weed into the diet of a North American herbivore. Evolution 41, 892–901 (1987).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    14.
    Bowers, M. D., Stamp, N. E. & Collinge, S. K. Early stage of host range expansion by a specialist herbivore Euphydryas phaeton. Ecology 73, 526–536 (1992).
    Article  Google Scholar 

    15.
    Severns, P. M. & Breed, G. A. Behavioral consequences of exotic host plant adoption and the differing roles of male harassment on female movement in two checkerspot butterflies. Behav. Ecol. Sociobiol. 68, 805–814 (2014).
    Article  Google Scholar 

    16.
    United States Fish and Wildlife Service. Endangered and threatened wildlife and plants; proposed designation of critical habitat for the bay checkerspot butterfly (Euphydryas editha bayensis); proposed rule. (2000).

    17.
    United States Fish and Wildlife Service. Endangered and threatened wildlife and plants; designation of critical habitat for the Quino checkerspot butterfly (Euphydryas editha quino). (2002).

    18.
    United States Fish and Wildlife Service. ESA Proposed Listing Taylor’s Checkerspot. Fed. Regist. 77, (2012).

    19.
    Ehrlich, P. R. & Hanski, I. On the wings of checkerspots: a model system for population biology. Oxford University Press (2004).

    20.
    Singer, M. C., Ng, D. & Thomas, C. D. Heritability of oviposition preference and its relationship to offspring performance within a single insect population. Evolution 42, 977–985 (1988).
    CAS  PubMed  Article  Google Scholar 

    21.
    Singer, M. C. & McBride, C. S. Multitrait, host-associated divergence among sets of butterfly populations: implications for reproductive isolation and ecological speciation. Evol. Int. J. Org. Evol. 64, 921–933 (2009).
    Article  Google Scholar 

    22.
    Peñuelas, J., Sardans, J., Stefanescu, C., Parella, T. & Filella, I. Lonicera implexa leaves bearing naturally laid eggs of the specialist herbivore Euphydryas aurinia have dramatically greater concentrations of iridoid glycosides than other leaves. J. Chem. Ecol. 32, 1925–1933 (2006).
    PubMed  Article  CAS  Google Scholar 

    23.
    Nieminen, M., Suomi, J., Nouhuys, S. V., Sauri, P. & Riekkola, M.-L. Effect of iridoid glycoside content on oviposition host plant choice and parasitism in a specialist herbivore. J. Chem. Ecol. 22 (2003).

    24.
    Bowers, M. D. Unpalatability as a defense strategy of Euphydryas phaeton (Lepidoptera: Nymphalidae). Evolution 34, 586–600 (1980).
    PubMed  Article  Google Scholar 

    25.
    Bowers, M. D. Unpalatability as a defense strategy of western checkerspot butterflies (Euphydryas Scudder, Nymphalidae). Evolution 35, 367–375 (1981).
    PubMed  Article  Google Scholar 

    26.
    Dobler, S., Petschenka, G. & Pankoke, H. Coping with toxic plant compounds–the insect’s perspective on iridoid glycosides and cardenolides. Phytochemistry 72, 1593–1604 (2011).
    CAS  PubMed  Article  Google Scholar 

    27.
    Bowers, M. D. & Stamp, N. E. Effects of plant age, genotype and herbivory on Plantago performance and chemistry. Ecology 74, 1778–1791 (1993).
    Article  Google Scholar 

    28.
    Dyer, L. A. & Deane Bowers, M. The importance of sequestered iridoid glycosides as a defense against an ant predator. J. Chem. Ecol. 22, 1527–1539 (1996).

    29.
    Dunwiddie, P. W. et al. Intertwined fates: Opportunities and challenges in the linked recovery of two rare species. Nat. Areas J. 36, 207–215 (2016).
    Article  Google Scholar 

    30.
    Stinson, D. Washington State Status Report for the Mazama Pocket Gopher, Streaked Horned Lark, and Taylor’s Checkerspot. Washington Department of Fish and Wildlife (2005).

    31.
    Cavers, P. B., Bassett, I. J. & Crompton, C. W. The biology of Canadian weeds 47. Plantago lanceolata L. Can. J. Plant Sci. 60, 1269–1282 (1980).

    32.
    Haan, N. L., Bakker, J. D., Dunwiddie, P. W. & Linders, M. J. Instar-specific effects of host plants on survival of endangered butterfly larvae. Ecol. Entomol. 43, 742–753 (2018).
    Article  Google Scholar 

    33.
    Danby, W. H. Food plant of Melitaea taylori Edw. Can. Entomol. 22, 121–122 (1890).
    Article  Google Scholar 

    34.
    Buckingham, D. A., Linders, M., Landa, C., Mullen, L. & LeRoy, C. Oviposition preference of endangered Taylor’s checkerspot butterflies (Euphydryas editha taylori) using native and non-native hosts. Northwest Sci. 90, 491–497 (2016).
    Article  Google Scholar 

    35.
    Mead, E. W. & Stermitz, F. R. Content of iridoid glycosides in different parts of Castilleja. Phytochemistry 32, 1155–1158 (1993).
    CAS  Article  Google Scholar 

    36.
    Barclay, E., Arnold, M., Anderson, M. J. & Shepherdson, D. Husbandry manual: Taylor’s checkerspot (Euphydryas editha taylori)) (Oregon Zoo, Portland OR, 2009).
    Google Scholar 

    37.
    R Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing (2020).

    38.
    Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, (2015).

    39.
    Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    40.
    Lenth, R. V. Least-Squares Means: The R package lsmeans. J. Stat. Softw. 69, (2016).

    41.
    Bowers, M. D. & Stamp, N. E. Effect of hostplant genotype and predators on iridoid glycoside content of pupae of a specialist insect herbivore, Junonia coenia (Nymphalidae). Biochem. Syst. 25, 571–580 (1997).
    CAS  Article  Google Scholar 

    42.
    Bowers, M. D. Hostplant suitability and defensive chemistry of the Catalpa sphinx Ceratomia catalpae. J. Chem. Ecol. 29, 2359–2367 (2003).
    CAS  PubMed  Article  Google Scholar 

    43.
    Oksanen, J. et al. Package ‘vegan’. Community Ecol. Package Version 2, 1–295 (2013).
    Google Scholar 

    44.
    Yoon, S. & Read, Q. Consequences of exotic host use: Impacts on Lepidoptera and a test of the ecological trap hypothesis. Oecologia 181, 985–996 (2016).
    ADS  PubMed  Article  Google Scholar 

    45.
    Cogni, R. Resistance to plant invasion? A native specialist herbivore shows preference for and higher fitness on an introduced host. Biotropica 42, 188–193 (2010).
    Article  Google Scholar 

    46.
    Agosta, S. J. & Klemens, J. A. Ecological fitting by phenotypically flexible genotypes: implications for species associations, community assembly and evolution. Ecol. Lett. 11, 1123–1134 (2008).
    PubMed  Article  Google Scholar 

    47.
    Bowers, M. D., Boockvar, K. & Collinge, S. K. Iridoid glycosides of Chelone glabra (Scrophulariaceae) and their sequestration by larvae of a Sawfly, Tenthredo grandis (Tenthredinidae). J. Chem. Ecol. 19, 815–815 (1993).
    CAS  PubMed  Article  Google Scholar 

    48.
    Singer, M. C. Quantification of host preference by manipulation of oviposition behavior in the butterfly Euphydryas editha. Oecologia 52, 224–229 (1982).
    ADS  PubMed  Article  Google Scholar 

    49.
    Parmesan, C., Singer, M. C. & Harris, I. A. N. Absence of adaptive learning from the oviposition foraging behaviour of a checkerspot butterfly. Anim. Behav. 50, 161–175 (1995).
    Article  Google Scholar 

    50.
    Quintero, C., Lampert, E. C. & Bowers, M. D. Time is of the essence: direct and indirect effects of plant ontogenetic trajectories on higher trophic levels. Ecology 95, 2589–2602 (2014).
    Article  Google Scholar 

    51.
    Gardner, D. R. & Stermitz, F. R. Host plant utilization and iridoid glycoside sequestration by Euphdryas anicia (Lepidoptera: Nymphalidae). J. Chem. Ecol. 14, 2147–2168 (1988).
    CAS  PubMed  Article  Google Scholar 

    52.
    Haan, N. L., Bakker, J. D. & Bowers, M. D. Hemiparasites can transmit indirect effects from their host plants to herbivores. Ecology 99, 399–410 (2018).
    PubMed  Article  Google Scholar 

    53.
    Haan, N. L. Ecological interactions between Euphydryas editha larvae and their host plants (University of Washington, Seattle, 2017).
    Google Scholar 

    54.
    Bowers, M. D. Aposematic caterpillars: life-styles of the warningly colored and unpalatable, in Caterpillars: ecological and evolutionary constraints on foraging (eds. Stamp, N.S., and Casey, T.M.). Chapman & Hall (1993).

    55.
    Theodoratus, D. H. & Bowers, M. D. Effects of sequestered iridoid glycosides on prey choice of the prairie wolf spider Lycosa carolinensis. J. Chem. Ecol. 25, 283–295 (1999).
    CAS  Article  Google Scholar 

    56.
    Cirak, C. et al. Phenological changes in the chemical content of wild and greenhouse-grown Hypericum pruinatum: hypericins, hyperforins and phenolic acids. Res Rev J Bot. 4, 37–47 (2015).
    ADS  Google Scholar 

    57.
    Richards, L. A. et al. Synergistic effects of iridoid glycosides on the survival, development and immune response of a specialist caterpillar, Junonia coenia (Nymphalidae). J. Chem. Ecol. 38, 1276–1284 (2012).
    CAS  PubMed  Article  Google Scholar 

    58.
    Smilanich, A. M., Dyer, L. A., Chambers, J. Q. & Bowers, M. D. Immunological cost of chemical defence and the evolution of herbivore diet breadth. Ecol. Lett. 12, 612–621 (2009).
    PubMed  Article  PubMed Central  Google Scholar 

    59.
    Hamilton, N.E. & Ferry, M. ggtern: Ternary diagrams using ggplot2. J. Stat. Softw., Code Snippets, 87, 1–17 (2018). More

  • in

    The impact of injury on apparent survival of whale sharks (Rhincodon typus) in South Ari Atoll Marine Protected Area, Maldives

    1.
    McCauley, D. J. et al. Marine defaunation: Animal loss in the global ocean. Science 347, 1255641 (2015).
    PubMed  Article  CAS  Google Scholar 
    2.
    Dulvy, N. K. et al. Extinction risk and conservation of the world’s sharks and rays. eLife 3, 590 (2014).
    Article  Google Scholar 

    3.
    Hutchings, J. A., Myers, R. A., García, V. B., Lucifora, L. O. & Kuparinen, A. Life-history correlates of extinction risk and recovery potential. Ecol. Appl. 22, 1061–1067 (2012).
    PubMed  Article  Google Scholar 

    4.
    Frisk, M. & Miller, T. J. Life histories and vulnerability to exploitation of elasmobranchs: Inferences from elasticity, perturbation and phylogenetic analyses. Artic. J. Northwest Atl. Fish. Sci. https://doi.org/10.2960/J.v35.m514 (2005).
    Article  Google Scholar 

    5.
    Carr, L. A. et al. Illegal shark fishing in the Galápagos Marine Reserve. Mar. Policy 39, 317–321 (2013).
    Article  Google Scholar 

    6.
    Dharmadi, F. & Satria, F. African Journal of Marine Science Fisheries management and conservation of sharks in Indonesia. Afr. J. Mar. Sci. 37, 249–258 (2015).
    Article  Google Scholar 

    7.
    Heupel, M., Carlson, J. & Simpfendorfer, C. Shark nursery areas: Concepts, definition, characterization and assumptions. Mar. Ecol. Prog. Ser. 337, 287–297 (2007).
    ADS  Article  Google Scholar 

    8.
    Meylan, P. A., Meylan, A. B. & Gray, J. A. The ecology and migrations of sea turtles 8. Tests of the developmental habitat hypothesis. Bull. Am. Museum Nat. Hist. 357, 1–70 (2011).
    Article  Google Scholar 

    9.
    Jennings, D. E., Gruber, S. H., Franks, B. R., Kessel, S. T. & Robertson, A. L. Effects of large-scale anthropogenic development on juvenile lemon shark (Negaprion brevirostris) populations of Bimini, Bahamas. Environ. Biol. Fishes 83, 369–377 (2008).
    Article  Google Scholar 

    10.
    Kinney, M. J. & Simpfendorfer, C. A. Reassessing the value of nursery areas to shark conservation and management. Conserv. Lett. 2, 53–60 (2009).
    Article  Google Scholar 

    11.
    Healy, T. J., Hill, N. J., Chin, A. & Barnett, A. A global review of elasmobranch tourism activities, management and risk. Mar. Policy 118, 103964 (2020).
    Article  Google Scholar 

    12.
    White, T. D. et al. Assessing the effectiveness of a large marine protected area for reef shark conservation. Biol. Conserv. 207, 64–71 (2017).
    Article  Google Scholar 

    13.
    Claudet, J., Loiseau, C., Sostres, M. & Correspondence, M. Z. Underprotected marine protected areas in a global biodiversity hotspot. One Earth https://doi.org/10.1016/j.oneear.2020.03.008 (2020).
    Article  Google Scholar 

    14.
    Pierce, S. & Norman, B. Rhincodon typus. IUCN Red List Threat. Species e-T19488A2, (2016).

    15.
    CITES. Convention on international trade in endangered species of wild fauna and flora. Amendments to Appendices I and II of CITES. (2000).

    16.
    Convention on Migratory Species. Proposal for the inclusion of the whale shark (Rhincodon typus) on Appendix I of the convention CMS convention on migratory species. (2017).

    17.
    Simpfendorfer, C. A. & Dulvy, N. K. Bright spots of sustainable shark fishing. Curr. Biol. 27, R97–R98 (2017).
    CAS  PubMed  Article  Google Scholar 

    18.
    Reeve-Arnold, K. E., Kinni, J., Newbigging, R., Pierce, S. J. & Roques, K. Sustaining whale shark tourism in a diminishing population. In (Hamad bin Khalifa University Press, HBKU Press, 2016). https://doi.org/10.5339/qproc.2016.iwsc4.49.

    19.
    Pravin, P. Whale Shark in the Indian Coast—Need for conservation. Curr. Sci. 79, 310–315 (2000).
    Google Scholar 

    20.
    Li, W., Wang, Y. & Norman, B. A preliminary survey of whale shark Rhincodon typus catch and trade in China: An emerging crisis. J. Fish Biol. 80, 1608–1618 (2012).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    21.
    Hearn, A. R. et al. Adult female whale sharks make long-distance movements past Darwin Island (Galapagos, Ecuador) in the Eastern Tropical Pacific. Mar. Biol. 163, 1–12 (2016).
    Article  Google Scholar 

    22.
    Wilson, S. G., Polovina, J. J., Stewart, B. S. & Meekan, M. G. Movements of whale sharks (Rhincodon typus) tagged at Ningaloo Reef, Western Australia. Mar. Biol. 148, 1157–1166 (2006).
    Article  Google Scholar 

    23.
    Hueter, R. E., Tyminski, J. P. & de la Parra, R. Horizontal movements, migration patterns, and population structure of whale sharks in the Gulf of Mexico and northwestern Caribbean Sea. PLoS ONE 8, e71883 (2013).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    24.
    Robinson, D. P. et al. Some like it hot: Repeat migration and residency of whale sharks within an extreme natural environment. PLoS ONE 12, e0185360 (2017).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    25.
    Araujo, G. et al. Photo-ID and telemetry highlight a global whale shark hotspot in Palawan, Philippines. Sci. Rep. 9, 1–12 (2019).
    Article  CAS  Google Scholar 

    26.
    Bradshaw, C. J. A., Fitzpatrick, B. M., Steinberg, C. C., Brook, B. W. & Meekan, M. G. Decline in whale shark size and abundance at Ningaloo Reef over the past decade: The world’s largest fish is getting smaller. Biol. Conserv. 141, 1894–1905 (2008).
    Article  Google Scholar 

    27.
    Speed, C. W. et al. Scarring patterns and relative mortality rates of Indian Ocean whale sharks. J. Fish Biol. 72, 1488–1503 (2008).
    Article  Google Scholar 

    28.
    Lester, E. et al. Multi-year patterns in scarring, survival and residency of whale sharks in Ningaloo Marine Park, Western Australia. Mar. Ecol. Prog. Ser. 634, 115–125 (2020).
    ADS  Article  Google Scholar 

    29.
    Rowat, D. & Brooks, K. S. A review of the biology, fisheries and conservation of the whale shark Rhincodon typus. J. Fish Biol. 80, 1019–1056 (2012).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    30.
    Cochran, J. E. M. et al. Multi-method assessment of whale shark (Rhincodon typus) residency, distribution, and dispersal behavior at an aggregation site in the Red Sea. PLoS ONE 14, e0222285 (2019).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    31.
    Copping, J. P., Stewart, B. D., McClean, C. J., Hancock, J. & Rees, R. Does bathymetry drive coastal whale shark (Rhincodon typus) aggregations?. PeerJ 6, e4904 (2018).
    PubMed  PubMed Central  Article  Google Scholar 

    32.
    Norman, B. M. et al. Undersea constellations: The global biology of an endangered marine megavertebrate further informed through citizen science. Bioscience 67, 1029–1043 (2017).
    Article  Google Scholar 

    33.
    Donati, G. et al. New insights into the South Ari atoll whale shark, Rhincodon typus, aggregation. In (Hamad bin Khalifa University Press, HBKU Press, 2016). https://doi.org/10.5339/qproc.2016.iwsc4.16.

    34.
    Riley, M. J., Hale, M. S., Harman, A. & Rees, R. G. Analysis of whale shark Rhincodon typus aggregations near South Ari Atoll, Maldives Archipelago. Aquat. Biol. 8, 145–150 (2010).
    Article  Google Scholar 

    35.
    Rowat, D., Meekan, M. G., Engelhardt, U., Pardigon, B. & Vely, M. Aggregations of juvenile whale sharks (Rhincodon typus) in the Gulf of Tadjoura, Djibouti. Environ. Biol. Fishes 80, 465–472 (2007).
    Article  Google Scholar 

    36.
    Cagua, E. F. et al. Acoustic telemetry reveals cryptic residency of whale sharks. Biol. Lett. 11, 20150092 (2015).
    PubMed  PubMed Central  Article  Google Scholar 

    37.
    Thomson, J. A. et al. Feeding the world’s largest fish: Highly variable whale shark residency patterns at a provisioning site in the Philippines. R. Soc. Open Sci. 4, 170394 (2017).
    ADS  PubMed  PubMed Central  Article  Google Scholar 

    38.
    Perry, C. T. et al. Comparing length-measurement methods and estimating growth parameters of free-swimming whale sharks (Rhincodon typus) near the South Ari Atoll, Maldives. Mar. Freshw. Res. 69, 1487 (2018).
    Article  Google Scholar 

    39.
    Riley, M. J., Harman, A. & Rees, R. G. Evidence of continued hunting of whale sharks Rhincodon typus in the Maldives. Environ. Biol. Fishes 86, 371–374 (2009).
    Article  Google Scholar 

    40.
    Cagua, E. F., Collins, N., Hancock, J. & Rees, R. Whale shark economics: A valuation of wildlife tourism in South Ari Atoll. Maldives. PeerJ 2, e515 (2014).
    PubMed  Article  Google Scholar 

    41.
    Arzoumanian, Z., Holmberg, J. & Norman, B. An astronomical pattern-matching algorithm for computer-aided identification of whale sharks Rhincodon typus. J. Appl. Ecol. 42, 999–1011 (2005).
    Article  Google Scholar 

    42.
    Bradshaw, C. J. A., Mollett, H. F. & Meekan, M. G. Inferring population trends for the world’s largest fish from mark recapture estimates of survival. J. Anim. Ecol. 76, 480–489 (2007).
    PubMed  Article  Google Scholar 

    43.
    Holmberg, J., Norman, B. & Arzoumanian, Z. Estimating population size, structure, and residency time for whale sharks Rhincodon typus through collaborative photo-identification. Endanger. Species Res. 7, 39–53 (2009).
    Article  Google Scholar 

    44.
    Rowat, D., Gore, M., Meekan, M. G., Lawler, I. R. & Bradshaw, C. J. A. Aerial survey as a tool to estimate whale shark abundance trends. J. Exp. Mar. Biol. Ecol. 368, 1–8 (2009).
    Article  Google Scholar 

    45.
    Acuña-Marrero, D. et al. Whale shark (Rhincodon typus) seasonal presence, residence time and habitat use at darwin island, galapagos marine reserve. PLoS ONE 9, e115946 (2014).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    46.
    Schwarz, C. J., Bailey, R. E., Irvine, J. R. & Dalziel, F. C. Estimating salmon spawning escapement using capture-recapture methods. Can. J. Fish. Aquat. Sci. 50, 1181–1197 (1993).
    Article  Google Scholar 

    47.
    Schwarz, C. J. & Arnason, A. N. A general methodology for the analysis of capture-recapture experiments in open populations. Biometrics 52, 860 (1996).
    MathSciNet  MATH  Article  Google Scholar 

    48.
    Whitehead, H. Analysis of animal movement using opportunistic individual identifications: Application to sperm whales. Ecology 82, 1417–1432 (2001).
    Article  Google Scholar 

    49.
    QGIS.org. QGIS Geographic Information System. Open Source Geospatial Foundation Project. (2020).

    50.
    Van Tienhoven, A. M., Den Hartog, J. E., Reijns, R. A. & Peddemors, V. M. A computer-aided program for pattern-matching of natural marks on the spotted raggedtooth shark Carcharias taurus. J. Appl. Ecol. 44, 273–280 (2007).
    Article  Google Scholar 

    51.
    RStudio Team. RStudio: Integrated Development for R. (2015).

    52.
    Laake, J. L. RMark: An R interface for analysis of capture-recapture data with MARK. AFSC Processed Rep. 2013-01 Alaska Fish. Sci. Cent., NOAA, Natl. Mar. Fish. Serv., (2013). https://doi.org/10.1017/CBO9781107415324.004.

    53.
    Schwarz, C., Arnason, A., Cooch, E. & White, G. Jolly-Seber models in MARK. Progr. MARK–a gentle Introd. 18th Ed. (2018).

    54.
    Cooch, E. & White, G. Program MARK: A gentle introduction (13th ed.). available online with MARK Program. (2006).

    55.
    Whitehead, H. SOCPROG programs: Analysing animal social structures. Behav. Ecol. Sociobiol. 63, 765–778 (2009).
    Article  Google Scholar 

    56.
    Whitehead, H. Selection of models of lagged identification rates and lagged association rates using AIC and QAIC. Commun. Stat. Simul. Comput. 36, 1233–1246 (2007).
    MathSciNet  MATH  Article  Google Scholar 

    57.
    Buckland, S. T. & Garthwaite, P. H. Quantifying precision of mark-recapture estimates using the bootstrap and related methods. Biometrics 47, 255 (1991).
    Article  Google Scholar 

    58.
    Rohner, C. A. et al. No place like home? High residency and predictable seasonal movement of whale sharks off Tanzania. Front. Mar. Sci. 7, 423 (2020).
    Article  Google Scholar 

    59.
    Norman, B. M., Whitty, J. M., Beatty, S. J., Reynolds, S. D. & Morgan, D. L. Do they stay or do they go? Acoustic monitoring of whale sharks at Ningaloo Marine Park, Western Australia. J. Fish Biol. 91, 1713–1720 (2017).
    CAS  PubMed  Article  Google Scholar 

    60.
    Araujo, G. et al. Population structure and residency patterns of whale sharks, Rhincodon typus, at a provisioning site in Cebu, Philippines. PeerJ 2014, e543 (2014).
    Article  Google Scholar 

    61.
    Prebble, C. et al. Limited latitudinal ranging of juvenile whale sharks in the Western Indian Ocean suggests the existence of regional management units. Mar. Ecol. Prog. Ser. 601, 167–183 (2018).
    ADS  Article  Google Scholar 

    62.
    Araujo, G. et al. Population structure and residency patterns of whale sharks, Rhincodon typus, at a provisioning site in Cebu, Philippines. PeerJ 2, e543 (2014).
    PubMed  PubMed Central  Article  Google Scholar 

    63.
    Akhilesh, K. V. et al. Landings of whale sharks Rhincodon typus Smith, 1828 in Indian waters since protection in 2001 through the Indian Wildlife (Protection) Act, 1972. Environ. Biol. Fishes 96, 713–722 (2013).
    Article  Google Scholar 

    64.
    Heyman, W., Graham, R., Kjerfve, B. & Johannes, R. Whale sharks Rhincodon typus aggregate to feed on fish spawn in Belize. Mar. Ecol. Prog. Ser. 215, 275–282 (2001).
    ADS  Article  Google Scholar 

    65.
    Meekan, M. et al. Population size and structure of whale sharks Rhincodon typus at Ningaloo Reef, Western Australia. Mar. Ecol. Prog. Ser. 319, 275–285 (2006).
    ADS  Article  Google Scholar 

    66.
    Cochran, J. E. M. et al. Population structure of a whale shark Rhincodon typus aggregation in the Red Sea. J. Fish Biol. 89, 1570–1582 (2016).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    67.
    Araujo, G. et al. Population structure, residency patterns and movements of whale sharks in Southern Leyte, Philippines: Results from dedicated photo-ID and citizen science. Aquat. Conserv. Mar. Freshw. Ecosyst. 27, 237–252 (2017).
    Article  Google Scholar 

    68.
    Robinson, D. P. et al. Population structure, abundance and movement of whale sharks in the Arabian Gulf and the Gulf of Oman. PLoS ONE 11, e0158593 (2016).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    69.
    McCoy, E. et al. Long-term photo-identification reveals the population dynamics and strong site fidelity of adult whale sharks to the coastal waters of Donsol, Philippines. Front. Mar. Sci. 5, 271 (2018).
    Article  Google Scholar 

    70.
    Araujo, G. et al. In-water methods reveal population dynamics of a green turtle Chelonia mydas foraging aggregation in the Philippines. Endanger. Species Res. 40, 207–218 (2019).
    Article  Google Scholar 

    71.
    Sleeman, J. C. et al. To go or not to go with the flow: Environmental influences on whale shark movement patterns. J. Exp. Mar. Biol. Ecol. 390, 84–98 (2010).
    Article  Google Scholar 

    72.
    Calambokidis, J., Laake, J. L. & Klimek, A. Abundance and population structure of seasonal gray whales in the Pacific Northwest, 1998–2008. Sc/62/Brg32, Vol. 2008 (2010).

    73.
    Branstetter, S. Early Life-History Implications of Selected Carcharhinoid and Lamnoid Sharks of the Northwest Atlantic. Elasmobranchs as Living Resour. Adv. Biol. Ecol. Syst. Status Fish. (1990).

    74.
    Parker, J. H. & Gischler, E. Modern foraminiferal distribution and diversity in two atolls from the Maldives, Indian Ocean. Mar. Micropaleontol. 78, 30–49 (2011).
    ADS  Article  Google Scholar 

    75.
    Halvorsen, M. B., Casper, B. M., Woodley, C. M., Carlson, T. J. & Popper, A. N. Threshold for onset of injury in Chinook salmon from exposure to impulsive pile driving sounds. PLoS ONE 7, e38968 (2012).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    76.
    Haskell, P. J. et al. Monitoring the effects of tourism on whale shark Rhincodon typus behaviour in Mozambique. ORYX 49, 492–499 (2015).
    Article  Google Scholar 

    77.
    Quiros, A. L. Tourist compliance to a Code of Conduct and the resulting effects on whale shark (Rhincodon typus) behavior in Donsol, Philippines. Fish. Res. 84, 102–108 (2007).
    Article  Google Scholar 

    78.
    Araujo, G., Vivier, F., Labaja, J. J., Hartley, D. & Ponzo, A. Assessing the impacts of tourism on the world’s largest fish Rhincodon typus at Panaon Island, Southern Leyte, Philippines. Aquat. Conserv. Mar. Freshw. Ecosyst. 27, 986–994 (2017).
    Article  Google Scholar 

    79.
    Finger, J. S. et al. Rate of movement of juvenile lemon sharks in a novel open field, are we measuring activity or reaction to novelty?. Anim. Behav. 116, 75–82 (2016).
    Article  Google Scholar 

    80.
    Cade, D. E. et al. Whale sharks increase swimming effort while filter feeding, but appear to maintain high foraging efficiencies. J. Exp. Biol. 223, jeb.224402 (2020).
    Article  Google Scholar 

    81.
    Archie, E. A. Wound healing in the wild: stress, sociality, and energetic costs affect wound healing in natural populations. Parasite Immunol. 35, n/a-n/a (2013).

    82.
    Baker, M. R., Swanson, P. & Young, G. Injuries from non-retention in gillnet fisheries suppress reproductive maturation in escaped fish. PLoS ONE 8, e69615 (2013).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    83.
    Neat, F. C., Taylor, A. C. & Huntingford, F. A. Proximate costs of fighting in male cichlid fish: The role of injuries and energy metabolism. Anim. Behav. 55, 875–882 (1998).
    CAS  PubMed  Article  Google Scholar 

    84.
    Meekan, M. G., Fuiman, L. A., Davis, R., Berger, Y. & Thums, M. Swimming strategy and body plan of the world’s largest fish: Implications for foraging efficiency and thermoregulation. Front. Mar. Sci. 2, 64 (2015).
    Article  Google Scholar 

    85.
    Chin, A., Mourier, J. & Rummer, J. L. Blacktip reef sharks (Carcharhinus melanopterus) show high capacity for wound healing and recovery following injury. Conserv. Physiol. 3(1) (2015).

    86.
    Tierney, K. B. & Farrell, A. P. The relationships between fish health, metabolic rate, swimming performance and recovery in return-run sockeye salmon, Oncorhynchus nerka (Walbaum). J. Fish Dis. 27, 663–671 (2004).
    CAS  PubMed  Article  Google Scholar 

    87.
    McGregor, F., Richardson, A. J., Armstrong, A. J., Armstrong, A. O. & Dudgeon, C. L. Rapid wound healing in a reef manta ray masks the extent of vessel strike. PLoS ONE 14, e0225681 (2019).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    88.
    Tort, L. Stress and immune modulation in fish. Dev. Comp. Immunol. 35, 1366–1375 (2011).
    CAS  PubMed  Article  Google Scholar 

    89.
    Mateus, A. P., Anjos, L., Cardoso, J. R. & Power, D. M. Chronic stress impairs the local immune response during cutaneous repair in gilthead sea bream (Sparus aurata L.). Mol. Immunol. 87, 267–283 (2017).
    CAS  PubMed  Article  Google Scholar 

    90.
    Environmental Protection Agency. Maldivian Whale Shark Tourist Encounter Guidelines. (2009).

    91.
    Leston, F. A. L. Monitoring Tourist Pressure on Whale Shark (Rhincodon typus) Behaviour in South Ari MPA, Maldive) Behaviour in South Ari MPA, Maldive (The University of Edinburgh, Edinburgh, 2016).
    Google Scholar 

    92.
    Kallsen, H. Regulation of Whale Shark Tourism: A Data Driven Approach for the South Ari Marine Protected Area (Syddansk Universitet, Odense, 2018).
    Google Scholar 

    93.
    Montero-Quintana, A. N., Vázquez-Haikin, J. A., Merkling, T., Blanchard, P. & Osorio-Beristain, M. Ecotourism impacts on the behaviour of whale sharks: An experimental approach. ORYX 54, 270–275 (2020).
    Article  Google Scholar 

    94.
    Bouyoucos, I. A., Simpfendorfer, C. A. & Rummer, J. L. Estimating oxygen uptake rates to understand stress in sharks and rays. Rev. Fish Biol. Fish. 29, 297–311 (2019).
    Article  Google Scholar 

    95.
    Semeniuk, C. A. D., Bourgeon, S., Smith, S. L. & Rothley, K. D. Hematological differences between stingrays at tourist and non-visited sites suggest physiological costs of wildlife tourism. Biol. Conserv. 142, 1818–1829 (2009).
    Article  Google Scholar 

    96.
    Van Rijn, J. A. & Reina, R. D. Distribution of leukocytes as indicators of stress in the Australian swellshark, Cephaloscyllium laticeps. Fish Shellfish Immunol. 29, 534–538 (2010).
    PubMed  Article  CAS  PubMed Central  Google Scholar 

    97.
    Barnett, A., Payne, N. L., Semmens, J. M. & Fitzpatrick, R. Ecotourism increases the field metabolic rate of whitetip reef sharks. Biol. Conserv. 199, 132–136 (2016).
    Article  Google Scholar 

    98.
    Mau, R. Managing for conservation and recreation: The Ningaloo whale shark experience. J. Ecotourism 7, 213–225 (2008).
    Article  Google Scholar 

    99.
    Martin, R. A. A review of behavioural ecology of whale sharks (Rhincodon typus). Fish. Res. 84, 10–16 (2007).
    ADS  Article  Google Scholar 

    100.
    Skomal, G. B. & Mandelman, J. W. The physiological response to anthropogenic stressors in marine elasmobranch fishes: A review with a focus on the secondary response. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 126, 146–155 (2012).
    Article  CAS  Google Scholar 

    101.
    Pankhurst, N. W. The endocrinology of stress in fish: An environmental perspective. Gen. Comp. Endocrinol. 170, 265–275 (2011).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    102.
    Renshaw, G. M. C., Kutek, A. K., Grant, G. D. & Anoopkumar-Dukie, S. Forecasting elasmobranch survival following exposure to severe stressors. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 126, 101–112 (2012).
    Article  CAS  Google Scholar 

    103.
    Lester, E. et al. Using an electronic monitoring system and photo identification to understand effects of tourism encounters on whale sharks in Ningaloo Marine Park. Tour. Mar. Environ. 14, 121–131 (2019).
    Article  Google Scholar  More