Phenotypic biomarkers of climatic impacts on declining insect populations: A key role for decadal drought, thermal buffering and amplification effects and host plant dynamics

Carnicer J., Stefanescu C., Vives-Ingla M., López C., Cortizas S., Wheat C., Vila R., Llusià J., Peñuelas J. (2019) Phenotypic biomarkers of climatic impacts on declining insect populations: A key role for decadal drought, thermal buffering and amplification effects and host plant dynamics. Journal of Animal Ecology. : 0-0.
Link
Doi: 10.1111/1365-2656.12933

Abstract:

Widespread population declines have been reported for diverse Mediterranean butterflies over the last three decades, and have been significantly associated with increased global change impacts. The specific landscape and climatic drivers of these declines remain uncertain for most declining species. Here, we analyse whether plastic phenotypic traits of a model butterfly species (Pieris napi) perform as reliable biomarkers of vulnerability to extreme temperature impacts in natural populations, showing contrasting trends in thermally exposed and thermally buffered populations. We also examine whether improved descriptions of thermal exposure of insect populations can be achieved by combining multiple information sources (i.e., integrating measurements of habitat thermal buffering, habitat thermal amplification, host plant transpiration, and experimental assessments of thermal death time (TDT), thermal avoidance behaviour (TAB) and thermally induced trait plasticity). These integrative analyses are conducted in two demographically declining and two non-declining populations of P. napi. The results show that plastic phenotypic traits (butterfly body mass and wing size) are reliable biomarkers of population vulnerability to extreme thermal conditions. Butterfly wing size is strongly reduced only in thermally exposed populations during summer drought periods. Laboratory rearing of these populations documented reduced wing size due to significant negative effects of increased temperatures affecting larval growth. We conclude that these thermal biomarkers are indicative of the population vulnerability to increasing global warming impacts, showing contrasting trends in thermally exposed and buffered populations. Thermal effects in host plant microsites significantly differ between populations, with stressful thermal conditions only effectively ameliorated in mid-elevation populations. In lowland populations, we observe a sixfold reduction in vegetation thermal buffering effects, and larval growth occurs in these populations at significantly higher temperatures. Lowland populations show reduced host plant quality (C/N ratio), reduced leaf transpiration rates and complete above-ground plant senescence during the peak of summer drought. Amplified host plant temperatures are observed in open microsites, reaching thermal thresholds that can affect larval survival. Overall, our results suggest that butterfly population vulnerability to long-term drought periods is associated with multiple co-occurring and interrelated ecological factors, including limited vegetation thermal buffering effects at lowland sites, significant drought impacts on host plant transpiration and amplified leaf surface temperature, as well as reduced leaf quality linked to the seasonal advance of plant phenology. Our results also identify multiannual summer droughts affecting larval growing periods as a key driver of the recently reported butterfly population declines in the Mediterranean biome. © 2018 The Authors. Journal of Animal Ecology © 2018 British Ecological Society

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Do asynchronies in extinction debt affect the structure of trophic networks? A case study of antagonistic butterfly larvae–plant networks

Guardiola M., Stefanescu C., Rod F., Pino J. (2018) Do asynchronies in extinction debt affect the structure of trophic networks? A case study of antagonistic butterfly larvae–plant networks. Oikos. 127: 803-813.
Link
Doi: 10.1111/oik.04536

Abstract:

Habitat loss and fragmentation affect species richness in fragmented habitats and can lead to immediate or time-delayed species extinctions. Asynchronies in extinction and extinction debt between interacting species may have severe effects on ecological networks. However, these effects remain largely unknown. We evaluated the effects of habitat patch and landscape changes on antagonistic butterfly larvae–plant trophic networks in Mediterranean grasslands in which previous studies had shown the existence of extinction debt in plants but not in butterflies. We sampled current species richness of habitat-specialist and generalist butterflies and vascular plants in 26 grasslands. We assessed the direct effects of historical and current patch and landscape characteristics on species richness and on butterfly larvae–plant trophic network metrics and robustness. Although positive species- and interactions–area relationships were found in all networks, structure and robustness was only affected by patch and landscape changes in networks involving the subset of butterfly specialists. Larger patches had more species (butterflies and host plants) and interactions but also more compartments, which decreased network connectance but increased network stability. Moreover, most likely due to the rescue effect, patch connectivity increased host-plant species (but not butterfly) richness and total links, and network robustness in specialist networks. On the other hand, patch area loss decreased robustness in specialist butterfly larvae–plant networks and made them more prone to collapse against host plant extinctions. Finally, in all butterfly larvae–plant networks we also detected a past patch and landscape effect on network asymmetry, which indicates that there were different extinction rates and extinction debts for butterflies and host plants. We conclude that asynchronies in extinction and extinction debt in butterfly–plant networks provoked by patch and landscape changes caused changes in species richness and network links in all networks, as well as changes in network structure and robustness in specialist networks. © 2017 The Authors

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Diversity of insect pollinators in the Iberian Peninsula [Diversidad de insectos polinizadores en la península ibérica]

Stefanescu C., Aguado L.O., Asís J.D., Baños-Picńn L., Cerdá X., Marcos García M.Á., Micń E., Ricarte A., Tormos J. (2018) Diversity of insect pollinators in the Iberian Peninsula [Diversidad de insectos polinizadores en la península ibérica]. Ecosistemas. 27: 9-22.
Link
Doi: 10.7818/ECOS.1391

Abstract:

Numerous observations and studies that have been carried out in recent decades show that, in addition to bees ((Hymenoptera; Anthophila), other groups of insects play a major role in entomophilous pollination. This article reviews the information and literature available on the contribution of the main groups of pollinators that traditionally have been considered as "secondary": beetles, butterflies and moths, dipterans, wasps and ants. For each of these groups a common outline is followed, with a brief introduction, a summary of the basic characteristics - both morphological and behavioral - in relation to pollination, their effectiveness as pollinators and their conservation status in the Iberian Peninsula. This review highlights the importance of all these groups in entomophilous pollination and the need to include them in comprehensive studies on this phenomenon. Although data are generally very limited, there is clear evidence of a general decline in most of these groups which calls for a pressing need to improve knowledge about their population trends. © 2018. Los Autores.

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Physiological differences between female limited, alternative life history strategies: The Alba phenotype in the butterfly Colias croceus

Woronik A., Stefanescu C., Käkelä R., Wheat C.W., Lehmann P. (2018) Physiological differences between female limited, alternative life history strategies: The Alba phenotype in the butterfly Colias croceus. Journal of Insect Physiology. 107: 257-264.
Link
Doi: 10.1016/j.jinsphys.2018.03.008

Abstract:

Across a wide range of taxa, individuals within populations exhibit alternative life history strategies (ALHS) where their phenotypes dramatically differ due to divergent investments in growth, reproduction and survivorship, with the resulting trade-offs directly impacting Darwinian fitness. Though the maintenance of ALHS within populations is fairly well understood, little is known regarding the physiological mechanisms that underlie ALHS and how environmental conditions can affect the evolution and expression of these phenotypes. One such ALHS, known as Alba, exists within females of many species in the butterfly genus Colias. Previous works in New World species not only found that female morphs differ in their wing color due to a reallocation of resources away from the synthesis of wing pigments to other areas of development, but also that temperature played an important role in these trade-offs. Here we build on previous work conducted in New World species by measuring life history traits and conducting lipidomics on individuals reared at hot and cold temperatures in the Old World species Colias croceus. Results suggest that the fitness of Alba and orange morphs likely varies with rearing temperature, where Alba females have higher fitness in cold conditions and orange in warm. Additionally shared traits between Old and New World species suggest the Alba mechanism is likely conserved across the genus. Finally, in the cold treatment we observe an intermediate yellow morph that may have decreased fitness due to slower larval development. This cost may manifest as disruptive selection in the field, thereby favoring the maintenance of the two discrete morphs. Taken together these results add insights into the evolution of, and the selection on, the Alba ALHS. © 2018 Elsevier Ltd

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Applicability of butterfly transect counts to estimate species richness in different parts of the palaearctic region

Zhang C., Harpke A., Kühn E., Páramo F., Settele J., Stefanescu C., Wiemers M., Zhang Y., Schweiger O. (2018) Applicability of butterfly transect counts to estimate species richness in different parts of the palaearctic region. Ecological Indicators. 95: 735-740.
Link
Doi: 10.1016/j.ecolind.2018.08.027

Abstract:

Transect counts are one of the most popular approaches to assess and monitor butterfly diversity, especially with the background of biodiversity loss. This method was developed in Europe, but its transferability is seldom tested across the world. To assess transferability, we compared butterfly richness estimates based on transect counts in Spain, Germany and central China, a region with a considerably different biogeographic history and more diverse butterfly fauna compared to Europe. We found that the efficiency of transect counts was much lower in China than in the other two regions. Apart from the fact that traditional transect counts may undersample canopy species which are predominant in central China, higher efficiency in Europe may be primarily attributed to different patterns of butterfly richness likely caused by different biogeographic and anthropogenic land-use history. Our results highlight that great caution is needed when transect count methods are transferred to other regions of the world, especially to particularly species rich areas with a high number of rare species. Low detectability of certain species can substantially mask species richness estimates, and we suggest to carefully adapt sampling effort and perhaps combine transect counts with other methods to ensure more realistic assessment of species richness in such regions. © 2018

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The database of the PREDICTS (Projecting Responses of Ecological Diversity In Changing Terrestrial Systems) project

Hudson, L.N., Newbold, T., Contu, S., Hill, S.L.L., Lysenko, I., De Palma, A., Phillips, H.R.P., Alhusseini, T.I., Bedford, F.E., Bennett, D.J., Booth, H., Burton, V.J., Chng, C.W.T., Choimes, A., Correia, D.L.P., Day, J., Echeverría-Londoño, S., Emerson, S.R., Gao, D., Garon, M., Harrison, M.L.K., Ingram, D.J., Jung, M., Kemp, V., Kirkpatrick, L., Martin, C.D., Pan, Y., Pask-Hale, G.D., Pynegar, E.L., Robinson, A.N., Sanchez-Ortiz, K., Senior, R.A., Simmons, B.I., White, H.J., Zhang, H., Aben, J., Abrahamczyk, S., Adum, G.B., Aguilar-Barquero, V., Aizen, M.A., Albertos, B., Alcala, E.L., del Mar Alguacil, M., Alignier, A., Ancrenaz, M., Andersen, A.N., Arbeláez-Cortés, E., Armbrecht, I., Arroyo-Rodríguez, V., Aumann, T., Axmacher, J.C., Azhar, B., Azpiroz, A.B., Baeten, L., Bakayoko, A., Báldi, A., Banks, J.E., Baral, S.K., Barlow, J., Barratt, B.I.P., Barrico, L., Bartolommei, P., Barton, D.M., Basset, Y., Batáry, P., Bates, A.J., Baur, B., Bayne, E.M., Beja, P., Benedick, S., Berg, Å., Bernard, H., Berry, N.J., Bhatt, D., Bicknell, J.E., Bihn, J.H., Blake, R.J., Bobo, K.S., Bóçon, R., Boekhout, T., Böhning-Gaese, K., Bonham, K.J., Borges, P.A.V., Borges, S.H., Boutin, C., Bouyer, J., Bragagnolo, C., Brandt, J.S., Brearley, F.Q., Brito, I., Bros, V., Brunet, J., Buczkowski, G., Buddle, C.M., Bugter, R., Buscardo, E., Buse, J., Cabra-García, J., Cáceres, N.C., Cagle, N.L., Calviño-Cancela, M., Cameron, S.A., Cancello, E.M., Caparrós, R., Cardoso, P., Carpenter, D., Carrijo, T.F., Carvalho, A.L., Cassano, C.R., Castro, H., Castro-Luna, A.A., Rolando, C.B., Cerezo, A., Chapman, K.A., Chauvat, M., Christensen, M., Clarke, F.M., Cleary, D.F.R., Colombo, G., Connop, S.P., Craig, M.D., Cruz-López, L., Cunningham, S.A., D'Aniello, B., D'Cruze, N., da Silva, P.G., Dallimer, M., Danquah, E., Darvill, B., Dauber, J., Davis, A.L.V., Dawson, J., de Sassi, C., de Thoisy, B., Deheuvels, O., Dejean, A., Devineau, J.-L., Diekötter, T., Dolia, J.V., Domínguez, E., Dominguez-Haydar, Y., Dorn, S., Draper, I., Dreber, N., Dumont, B., Dures, S.G., Dynesius, M., Edenius, L., Eggleton, P., Eigenbrod, F., Elek, Z., Entling, M.H., Esler, K.J., de Lima, R.F., Faruk, A., Farwig, N., Fayle, T.M., Felicioli, A., Felton, A.M., Fensham, R.J., Fernandez, I.C., Ferreira, C.C., Ficetola, G.F., Fiera, C., Filgueiras, B.K.C., Fırıncıoğlu, H.K., Flaspohler, D., Floren, A., Fonte, S.J., Fournier, A., Fowler, R.E., Franzén, M., Fraser, L.H., Fredriksson, G.M., Freire, G.B., Frizzo, T.L.M., Fukuda, D., Furlani, D., Gaigher, R., Ganzhorn, J.U., García, K.P., Garcia-R, J.C., Garden, J.G., Garilleti, R., Ge, B.-M., Gendreau-Berthiaume, B., Gerard, P.J., Gheler-Costa, C., Gilbert, B., Giordani, P., Giordano, S., Golodets, C., Gomes, L.G.L., Gould, R.K., Goulson, D., Gove, A.D., Granjon, L., Grass, I., Gray, C.L., Grogan, J., Gu, W., Guardiola, M., Gunawardene, N.R., Gutierrez, A.G., Gutiérrez-Lamus, D.L., Haarmeyer, D.H., Hanley, M.E., Hanson, T., Hashim, N.R., Hassan, S.N., Hatfield, R.G., Hawes, J.E., Hayward, M.W., Hébert, C., Helden, A.J., Henden, J.-A., Henschel, P., Hernández, L., Herrera, J.P., Herrmann, F., Herzog, F., Higuera-Diaz, D., Hilje, B., Höfer, H., Hoffmann, A., Horgan, F.G., Hornung, E., Horváth, R., Hylander, K., Isaacs-Cubides, P., Ishida, H., Ishitani, M., Jacobs, C.T., Jaramillo, V.J., Jauker, B., Hernández, F.J., Johnson, M.F., Jolli, V., Jonsell, M., Juliani, S.N., Jung, T.S., Kapoor, V., Kappes, H., Kati, V., Katovai, E., Kellner, K., Kessler, M., Kirby, K.R., Kittle, A.M., Knight, M.E., Knop, E., Kohler, F., Koivula, M., Kolb, A., Kone, M., Kőrösi, Á., Krauss, J., Kumar, A., Kumar, R., Kurz, D.J., Kutt, A.S., Lachat, T., Lantschner, V., Lara, F., Lasky, J.R., Latta, S.C., Laurance, W.F., Lavelle, P., Le Féon, V., LeBuhn, G., Légaré, J.-P., Lehouck, V., Lencinas, M.V., Lentini, P.E., Letcher, S.G., Li, Q., Litchwark, S.A., Littlewood, N.A., Liu, Y., Lo-Man-Hung, N., López-Quintero, C.A., Louhaichi, M., Lövei, G.L., Lucas-Borja, M.E., Luja, V.H., Luskin, M.S., MacSwiney G, M.C., Maeto, K., Magura, T., Mallari, N.A., Malone, L.A., Malonza, P.K., Malumbres-Olarte, J., Mandujano, S., Måren, I.E., Marin-Spiotta, E., Marsh, C.J., Marshall, E.J.P., Martínez, E., Martínez Pastur, G., Moreno Mateos, D., Mayfield, M.M., Mazimpaka, V., McCarthy, J.L., McCarthy, K.P., McFrederick, Q.S., McNamara, S., Medina, N.G., Medina, R., Mena, J.L., Mico, E., Mikusinski, G., Milder, J.C., Miller, J.R., Miranda-Esquivel, D.R., Moir, M.L., Morales, C.L., Muchane, M.N., Muchane, M., Mudri-Stojnic, S., Munira, A.N., Muoñz-Alonso, A., Munyekenye, B.F., Naidoo, R., Naithani, A., Nakagawa, M., Nakamura, A., Nakashima, Y., Naoe, S., Nates-Parra, G., Navarrete Gutierrez, D.A., Navarro-Iriarte, L., Ndang'ang'a, P.K., Neuschulz, E.L., Ngai, J.T., Nicolas, V., Nilsson, S.G., Noreika, N., Norfolk, O., Noriega, J.A., Norton, D.A., Nöske, N.M., Nowakowski, A.J., Numa, C., O'Dea, N., O'Farrell, P.J., Oduro, W., Oertli, S., Ofori-Boateng, C., Oke, C.O., Oostra, V., Osgathorpe, L.M., Otavo, S.E., Page, N.V., Paritsis, J., Parra-H, A., Parry, L., Pe'er, G., Pearman, P.B., Pelegrin, N., Pélissier, R., Peres, C.A., Peri, P.L., Persson, A.S., Petanidou, T., Peters, M.K., Pethiyagoda, R.S., Phalan, B., Philips, T.K., Pillsbury, F.C., Pincheira-Ulbrich, J., Pineda, E., Pino, J., Pizarro-Araya, J., Plumptre, A.J., Poggio, S.L., Politi, N., Pons, P., Poveda, K., Power, E.F., Presley, S.J., Proença, V., Quaranta, M., Quintero, C., Rader, R., Ramesh, B.R., Ramirez-Pinilla, M.P., Ranganathan, J., Rasmussen, C., Redpath-Downing, N.A., Reid, J.L., Reis, Y.T., Rey Benayas, J.M., Rey-Velasco, J.C., Reynolds, C., Ribeiro, D.B., Richards, M.H., Richardson, B.A., Richardson, M.J., Ríos, R.M., Robinson, R., Robles, C.A., Römbke, J., Romero-Duque, L.P., Rös, M., Rosselli, L., Rossiter, S.J., Roth, D.S., Roulston, T.H., Rousseau, L., Rubio, A.V., Ruel, J.-C., Sadler, J.P., Sáfián, S., Saldaña-Vázquez, R.A., Sam, K., Samnegård, U., Santana, J., Santos, X., Savage, J., Schellhorn, N.A., Schilthuizen, M., Schmiedel, U., Schmitt, C.B., Schon, N.L., Schüepp, C., Schumann, K., Schweiger, O., Scott, D.M., Scott, K.A., Sedlock, J.L., Seefeldt, S.S., Shahabuddin, G., Shannon, G., Sheil, D., Sheldon, F.H., Shochat, E., Siebert, S.J., Silva, F.A.B., Simonetti, J.A., Slade, E.M., Smith, J., Smith-Pardo, A.H., Sodhi, N.S., Somarriba, E.J., Sosa, R.A., Soto Quiroga, G., St-Laurent, M.-H., Starzomski, B.M., Stefanescu, C., Steffan-Dewenter, I., Stouffer, P.C., Stout, J.C., Strauch, A.M., Struebig, M.J., Su, Z., Suarez-Rubio, M., Sugiura, S., Summerville, K.S., Sung, Y.-H., Sutrisno, H., Svenning, J.-C., Teder, T., Threlfall, C.G., Tiitsaar, A., Todd, J.H., Tonietto, R.K., Torre, I., Tóthmérész, B., Tscharntke, T., Turner, E.C., Tylianakis, J.M., Uehara-Prado, M., Urbina-Cardona, N., Vallan, D., Vanbergen, A.J., Vasconcelos, H.L., Vassilev, K., Verboven, H.A.F., Verdasca, M.J., Verdú, J.R., Vergara, C.H., Vergara, P.M., Verhulst, J., Virgilio, M., Vu, L.V., Waite, E.M., Walker, T.R., Wang, H.-F., Wang, Y., Watling, J.I., Weller, B., Wells, K., Westphal, C., Wiafe, E.D., Williams, C.D., Willig, M.R., Woinarski, J.C.Z., Wolf, J.H.D., Wolters, V., Woodcock, B.A., Wu, J., Wunderle, J.M., Yamaura, Y., Yoshikura, S., Yu, D.W., Zaitsev, A.S., Zeidler, J., Zou, F., Collen, B., Ewers, R.M., Mace, G.M., Purves, D.W., Scharlemann, J.P.W., Purvis, A. (2017) The database of the PREDICTS (Projecting Responses of Ecological Diversity In Changing Terrestrial Systems) project. Ecology and Evolution. 7: 145-188.
Link
Doi: 10.1002/ece3.2579

Abstract:

European butterfly populations vary in sensitivity to weather across their geographical ranges

Mills, S.C., Oliver, T.H., Bradbury, R.B., Gregory, R.D., Brereton, T., Kühn, E., Kuussaari, M., Musche, M., Roy, D.B., Schmucki, R., Stefanescu, C., van Swaay, C., Evans, K.L. (2017) European butterfly populations vary in sensitivity to weather across their geographical ranges. Global Ecology and Biogeography. 26: 1374-1385.
Link
Doi: 10.1111/geb.12659

Abstract:

Impacts of global change on Mediterranean forests and their services

Peñuelas, J., Sardans, J., Filella, I., Estiarte, M., Llusià, J., Ogaya, R., Carnicer, J., Bartrons, M., Rivas-Ubach, A., Grau, O., Peguero, G., Margalef, O., Pla-Rabés, S., Stefanescu, C., Asensio, D., Preece, C., Liu, L., Verger, A., Barbeta, A., Achotegui-Castells, A., Gargallo-Garriga, A., Sperlich, D., Farré-Armengol, G., Fernández-Martínez, M., Liu, D., Zhang, C., Urbina, I., Camino-Serrano, M., Vives-Ingla, M., Stocker, B.D., Balzarolo, M., Guerrieri, R., Peaucelle, M., Marañón-Jiménez, S., Bórnez-Mejías, K., Mu, Z., Descals, A., Castellanos, A., Terradas, J. (2017) Impacts of global change on Mediterranean forests and their services. Forests. 8: 0-0.
Link
Doi: 10.3390/f8120463

Abstract:

Effects of organic and conventional crop management on vineyard biodiversity

Puig-Montserrat X., Stefanescu C., Torre I., Palet J., Fàbregas E., Dantart J., Arrizabalaga A., Flaquer C. (2017) Effects of organic and conventional crop management on vineyard biodiversity. Agriculture, Ecosystems and Environment. 243: 19-26.
Link
Doi: 10.1016/j.agee.2017.04.005

Abstract:

Although organic farming is rapidly expanding in the vineyards of southern Europe, conventional crop management, using treatments that require a number of chemical inputs to guarantee yields is still the most common approach to crop management. To gauge the effects of these management systems on biodiversity, communities of vascular plants, butterflies, moths and birds were studied in vineyards in the Priorat Appellation of Origin (Catalonia, NE Spain). Measurements inside plots (all four taxonomic groups) and in grass strips between crop lines (only butterflies and vascular plants) were taken in organically and non-organically treated vineyards. Crop treatment was found to have an important effect, stronger on the most sessile organisms. Organic farms hosted consistently richer communities of both vascular plants and butterflies, a trend that was also observed − albeit less significantly − in moths. The weaker response in this group was probably due to insufficient sampling. Birds, the most vagile of the surveyed taxa, showed no significant response to treatments. Grass strips acted in all cases as reservoirs of biodiversity and hosted richer assemblages. The current trend of placing vineyards on slopes without terracing should ensure the existence of uncultivated strips within the vineyards to enhance the biodiversity of these agroecosystems. As well, parameters such as altitude and urban surface area are important drivers of biodiversity in this region. Our results suggest that organic farming may contribute to halting the widespread decrease that is occurring in communities of butterflies and other insects in this region. © 2017 Elsevier B.V.

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Back to Africa: autumn migration of the painted lady butterfly Vanessa cardui is timed to coincide with an increase in resource availability

Stefanescu, C., Puig-Montserrat, X., Samraoui, B., Izquierdo, R., Ubach, A., Arrizabalaga, A. (2017) Back to Africa: autumn migration of the painted lady butterfly Vanessa cardui is timed to coincide with an increase in resource availability. Ecological Entomology. 42: 737-747.
Link
Doi: 10.1111/een.12442

Abstract:

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