Long-term phenological trends, species accumulation rates, aphid traits and climate: five decades of change in migrating aphids

1. Aphids represent a significant challenge to food production. The Rothamsted Insect Survey (RIS) runs a network of 12·2-m suction-traps throughout the year to collect migrating aphids. In 2014, the RIS celebrated its 50th anniversary. This paper marks that achievement with an extensive spatiotemporal analysis and the provision of the first British annotated checklist of aphids since 1964. 2. Our main aim was to elucidate mechanisms that advance aphid phenology under climate change and explain these using life-history traits. We then highlight emerging pests using accumulation patterns. 3. Linear and nonlinear mixed-effect models estimated the average rate of change per annum and effects of climate on annual counts, first and last flights and length of flight season since 1965. Two climate drivers were used: the accumulated day degrees above 16 °C (ADD16) indicated the potential for migration during the aphid season; the North Atlantic Oscillation (NAO) signalled the severity of the winter before migration took place. 4. All 55 species studied had earlier first flight trends at rate of β = −0·611 ± SE 0·015 days year−1. Of these species, 49% had earlier last flights, but the average species effect appeared relatively stationary (β = −0·010 ± SE 0·022 days year−1). Most species (85%) showed increasing duration of their flight season (β = 0·336 ± SE 0·026 days year−1), even though only 54% increased their log annual count (β = 0·002 ± SE <0·001 year−1). 5. The ADD16 and NAO were shown to drive patterns in aphid phenology in a spatiotemporal context. Early in the year when the first aphids were migrating, the effect of the winter NAO was highly significant. Further into the year, ADD16 was a strong predictor. Latitude had a near linear effect on first flights, whereas longitude produced a generally less-clear effect on all responses. Aphids that are anholocyclic (permanently parthenogenetic) or are monoecious (non-host-alternating) were advancing their phenology faster than those that were not. 6. Climate drives phenology and traits help explain how this takes place biologically. Phenology and trait ecology are critical to understanding the threat posed by emerging pests such as Myzus persicae nicotianae and Aphis fabae cirsiiacanthoidis, as revealed by the species accumulation analysis.

[1]  L. Taylor,et al.  COMPARATIVE SYNOPTIC DYNAMICS. I. RELATIONSHIPS BETWEEN INTER- AND INTRA-SPECIFIC SPATIAL AND TEMPORAL VARIANCE/MEAN POPULATION PARAMETERS , 1982 .

[2]  I. Woiwod,et al.  Flying in the face of change , 1994 .

[3]  Angus Westgarth-Smith,et al.  Temporal variations in English Populations of a forest insect pest, the green spruce aphid (Elatobium abietinum), associated with the North Atlantic Oscillation and global warming , 2007 .

[4]  G. M. Tatchell,et al.  The Rothamsted insect survey 12-metrë suction trap , 1988 .

[5]  O Hammer-Muntz,et al.  PAST: paleontological statistics software package for education and data analysis version 2.09 , 2001 .

[6]  J. Fletcher,et al.  IMPLICATIONS OF APHID FLIGHT PATTERNS FOR PEST MANAGEMENT OF POTATOES , 2000 .

[7]  Simon R. Leather,et al.  Individuals, populations and patterns in ecology. , 1994 .

[8]  L. Taylor,et al.  Insect migration, flight periodicity and the boundary layer , 1974 .

[9]  K. Frank,et al.  Temporal dynamics within a contemporary latitudinal diversity gradient. , 2008, Ecology letters.

[10]  R. Blackman,et al.  Aphids on the world's herbaceous plants and shrubs. Volume 1: host lists and keys. Volume 2: the aphids. , 2006 .

[11]  A. Dixon,et al.  Ecology of host alternation in aphids , 2013 .

[12]  H. Stroyan Additions to the British aphid fauna (Homoptera: Aphidoidea) , 1979 .

[13]  A. Mysterud,et al.  Review article. Studying climate effects on ecology through the use of climate indices: the North Atlantic Oscillation, El Niño Southern Oscillation and beyond , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[14]  C. Perrins,et al.  Effects of elevated temperature on multi‐species interactions: the case of Pedunculate Oak, Winter Moth and Tits , 1999 .

[15]  Rik Leemans,et al.  Faculty Opinions recommendation of European phenological response to climate change matches the warming pattern. , 2006 .

[16]  R. Harrington,et al.  Foresight from hindsight: the Rothamsted Insect Survey , 2007 .

[17]  T. Sparks,et al.  Climate change and trophic interactions. , 1999, Trends in ecology & evolution.

[18]  Bernt-Erik Sæther,et al.  Population Growth in a Wild Bird Is Buffered Against Phenological Mismatch , 2013, Science.

[19]  A. Dixon,et al.  Aphid Ecology An optimization approach , 1985, Springer Netherlands.

[20]  J. Pickup,et al.  Mortality during dispersal and the cost of host‐specificity in parasites: how many aphids find hosts? , 1998 .

[21]  O. Heie The Aphidoidea (Hemiptera) of Fennoscandia and Denmark, Volume 1. General Part. The Families Mindaridae, Hormaphididae, Thelaxidae, Anoeciidae, and Pemphigidae , 1980 .

[22]  W. A. Stevens Transmission of Plant Viruses , 1983 .

[23]  R. Blackman Variation in the photoperiodic response within natural populations of Myzus persicae (Sulz.). , 1971, Bulletin of entomological research.

[24]  Wolfgang W. Weisser,et al.  Aphid Movement: Process and Consequences , 2007 .

[25]  S. Leather Aphids on the world's trees: An identification and information guide: By R. L. Blackman and V. F. Eastop. Hardback (987 pp; £99.00). Wallingford, CAB International , 1996 .

[26]  R. Harrington,et al.  Trends in the Timings of the Start and End of Annual Flight Periods , 2010 .

[27]  S. Schneider,et al.  Fingerprints of global warming on wild animals and plants , 2003, Nature.

[28]  Susan P. Worner,et al.  Geographical location, climate and land use influences on the phenology and numbers of the aphid, Myzus persicae, in Europe , 2005 .

[29]  Toke Thomas Høye,et al.  The effects of phenological mismatches on demography , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[30]  D. Musolin Insects in a warmer world: ecological, physiological and life‐history responses of true bugs (Heteroptera) to climate change , 2007 .

[31]  S. Worner,et al.  Predicting spring migration of the damson-hop aphid Phorodon humuli (Homoptera: Aphididae) from historical records of host-plant flowering phenology and weather , 1995 .

[32]  Sue J. Welham,et al.  The trait and host plant ecology of aphids and their distribution and abundance in the United Kingdom , 2012 .

[33]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[34]  Aaron Christ,et al.  Mixed Effects Models and Extensions in Ecology with R , 2009 .

[35]  Marcel E Visser,et al.  Shifts in phenology due to global climate change: the need for a yardstick , 2005, Proceedings of the Royal Society B: Biological Sciences.

[36]  J. Michaud Implications of Climate Change for Cereal Aphids on the Great Plains of North America , 2010 .

[37]  Ian P. Woiwod,et al.  Long‐term changes in the abundance of flying insects , 2009 .

[38]  A. Dixon,et al.  Life cycles and polymorphism. , 2007 .

[39]  Ø. Hammer,et al.  PAST: PALEONTOLOGICAL STATISTICAL SOFTWARE PACKAGE FOR EDUCATION AND DATA ANALYSIS , 2001 .

[40]  S. Juliano,et al.  POPULATION DYNAMICS , 2007, Journal of the American Mosquito Control Association.

[41]  A. Dewar,et al.  Aerial migrations of the rose‐grain aphid, Metopolophium dirhodum(Wlk.), over Europe in 1979 , 1980 .

[42]  Sergio A. Estay,et al.  Non-linear feedback processes and a latitudinal gradient in the climatic effects determine green spruce aphid outbreaks in the UK , 2008 .

[43]  Geir Ottersen,et al.  Climate and the match or mismatch between predator requirements and resource availability , 2007 .

[44]  Synoptic monitoring for migrant insect pests in Great Britain and Western Europe VI: revised nomenclature for aphids and moths, analytical tables for spatial and temporalspecies parameters and light trap sampling site distributions , 1984 .

[45]  C. G. Johnson The Distribution of Insects in the Air and the Empirical Relation of Density to Height , 1957 .

[46]  Ian P. Woiwod,et al.  Effects of temperature on aphid phenology , 1995 .

[47]  B T Grenfell,et al.  Age, sex, density, winter weather, and population crashes in Soay sheep. , 2001, Science.

[48]  Steve Cafferty,et al.  Big hitting collectors make massive and disproportionate contribution to the discovery of plant species , 2012, Proceedings of the Royal Society B: Biological Sciences.

[49]  M. Lima,et al.  Northern Atlantic Oscillation effects on the temporal and spatial dynamics of green spruce aphid populations in the UK. , 2007, The Journal of animal ecology.

[50]  Daniel S. Chapman Greater phenological sensitivity to temperature on higher Scottish mountains: new insights from remote sensing , 2013, Global change biology.

[51]  J. Newman Climate change and the fate of cereal aphids in Southern Britain , 2005 .

[52]  H. Stroyan Aphids - Pterocommatinae and Aphidinae (Aphidini). Homoptera, Aphididae. , 1984 .

[53]  Sue J. Welham,et al.  Likelihood Ratio Tests for Fixed Model Terms using Residual Maximum Likelihood , 1997 .

[54]  R. L. Blackman,et al.  Aphids on the World's Crops: An Identification and Information Guide , 1984 .

[55]  Franklin B. Schwing,et al.  The Pace of Shifting Climate in Marine and Terrestrial Ecosystems , 2011, Science.

[56]  N. Moran,et al.  Molecular data support a rapid radiation of aphids in the Cretaceous and multiple origins of host alternation , 2000 .

[57]  J. Hardie,et al.  Flight behaviour of the bird cherry aphid, Rhopalosiphum padi , 1991 .

[58]  R. Messing,et al.  Morphological and ecological traits promoting aphid colonization of the Hawaiian Islands , 2006, Biological Invasions.

[59]  Kevin J Gaston,et al.  Predicting unknown species numbers using discovery curves , 2007, Proceedings of the Royal Society B: Biological Sciences.

[60]  J. Perry,et al.  Comparative phenologies of two migrant cereal aphid species , 1992 .

[61]  A. Miller‐Rushing,et al.  Forecasting phenology: from species variability to community patterns. , 2012, Ecology letters.

[62]  Tim G. Benton,et al.  Linking agricultural practice to insect and bird populations: a historical study over three decades , 2002 .

[63]  C. H. Lindroth Handbooks for the identification of British insects. Coleoptera, Carabidae. , 1974 .

[64]  Sue J. Welham,et al.  Environmental change and the phenology of European aphids , 2007 .

[65]  G. S. Kloet,et al.  A Check List of British Insects , 1946, Nature.

[66]  R. Tibshirani,et al.  Generalized Additive Models , 1986 .

[67]  T. Clutton‐Brock,et al.  Trophic level asynchrony in rates of phenological change for marine, freshwater and terrestrial environments , 2010 .

[68]  Paul J. CaraDonna,et al.  Phenological overlap of interacting species in a changing climate: an assessment of available approaches , 2013, Ecology and evolution.

[69]  P. Kindlmann,et al.  Dynamics of Production of Sexual Forms in Aphids: Theoretical and Experimental Evidence for Adaptive “Coin‐Flipping” Plasticity , 2004, The American Naturalist.

[70]  R. Harrington The Rothamsted Insect Survey strikes gold , 2014 .

[71]  F. Altermatt Temperature‐related shifts in butterfly phenology depend on the habitat , 2012 .