Phenology of forest caterpillars and their host trees: the importance of synchrony.

For many leaf-feeding herbivores, synchrony in phenology with their host plant is crucial as development outside a narrow phenological time window has severe fitness consequences. In this review, we link mechanisms, adaptation, and population dynamics within a single conceptual framework, needed for a full understanding of the causes and consequences of this synchrony. The physiological mechanisms underlying herbivore and plant phenology are affected by environmental cues, such as photoperiod and temperature, although not necessarily in the same way. That these different mechanisms lead to synchrony, even if there is spatial and temporal variation in plant phenology, is a result of the strong natural selection acting on the mechanism underlying herbivore phenology. Synchrony has a major impact on the population densities of leaf-feeding Lepidoptera, and years with a high synchrony may lead to outbreaks. Global climate change leads to a disruption of the synchrony between herbivores and their host plants, which may have major impacts for population viability if natural selection is insufficient to restore synchrony.

[1]  Marcel E. Visser,et al.  Predicting adaptation of phenology in response to climate change, an insect herbivore example , 2007 .

[2]  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.

[3]  H. Häggman,et al.  Growth and defense in deciduous trees and shrubs under UV-B. , 2005, Environmental pollution.

[4]  B. Kovanci,et al.  Pheromone trap catches of the olive moth, Prays oleae (Bern.) (Lep., Plutellidae) in relation to olive phenology and degree‐day models , 2005 .

[5]  L. Kajfez-Bogataj,et al.  Impact of Climate Change on Developmental Dynamics of Thrips tabaci (Thysanoptera: Thripidae): Can It Be Quantified? , 2005 .

[6]  D. E. Stevenson,et al.  Physiological Time Model of Scirpophaga incertulas (Lepidoptera: Pyralidae) in Rice in Guandong Province, People’s Republic of China , 2005, Journal of economic entomology.

[7]  James A Powell,et al.  Insect seasonality: circle map analysis of temperature-driven life cycles. , 2005, Theoretical population biology.

[8]  E. Grafton-Cardwell,et al.  Effects of temperature on development of vedalia beetle, Rodolia cardinalis (Mulsant) , 2005 .

[9]  S. Mopper Phenology — how time creates spatial structure in endophagous insect populations , 2005 .

[10]  E. Haukioja Plant defenses and population fluctuations of forest defoliators : mechanism-based scenarios , 2005 .

[11]  J. Strengbom,et al.  Do multitrophic interactions override N fertilization effects on Operophtera larvae? , 2005, Oecologia.

[12]  T. Kawecki,et al.  Conceptual issues in local adaptation , 2004 .

[13]  T. Rafoss,et al.  Can sunspot activity and ultraviolet–B radiation explain cyclic outbreaks of forest moth pest species? , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[14]  O. Junttila,et al.  Low temperature sensing in silver birch (Betula pendula Roth) ecotypes , 2004 .

[15]  S. Louda,et al.  Phenological synchrony affects interaction strength of an exotic weevil with Platte thistle, a native host plant , 2004, Oecologia.

[16]  J. Kunkel,et al.  Effects of maternal nutrition and egg provisioning on parameters of larval hatch, survival and dispersal in the gypsy moth, Lymantria dispar L. , 1996, Oecologia.

[17]  S. Harrison Resources and dispersal as factors limiting a population of the tussock moth (Orgyia vetusta), a flightless defoliator , 1994, Oecologia.

[18]  R. Dewar,et al.  Predicted changes in the synchrony of larval emergence and budburst under climatic warming , 1992, Oecologia.

[19]  A. Watt,et al.  Outbreaks of the winter moth on Sitka Spruce in Scotland are not influenced by nutrient deficiencies of trees, tree budburst, or pupal predation , 1991, Oecologia.

[20]  D. Lincoln The influence of plant carbon dioxide and nutrient supply on susceptibility to insect herbivores , 2004, Vegetatio.

[21]  H. Numata,et al.  Timing of diapause induction and its life‐history consequences in Nezara viridula: is it costly to expand the distribution range? , 2003 .

[22]  T. Klemola,et al.  Performance of a spring‐feeding moth in relation to time of oviposition and bud‐burst phenology of different host species , 2003 .

[23]  Olli-Pekka Tikkanen,et al.  Phenological variation as protection against defoliating insects: the case of Quercus robur and Operophtera brumata , 2003, Oecologia.

[24]  Jörg Schaber,et al.  Physiology-based phenology models for forest tree species in Germany , 2003, International journal of biometeorology.

[25]  J. Senn,et al.  Performance of the cyclic autumnal moth, Epirrita autumnata, in relation to birch mast seeding , 2003, Oecologia.

[26]  G. Yohe,et al.  A globally coherent fingerprint of climate change impacts across natural systems , 2003, Nature.

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

[28]  D. Denlinger,et al.  Regulation of diapause. , 2003, Annual review of entomology.

[29]  M. Visser,et al.  Great tits can reduce caterpillar damage in apple orchards , 2002 .

[30]  Atle Mysterud,et al.  Climate, changing phenology, and other life history traits: Nonlinearity and match–mismatch to the environment , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[31]  M. Noguer,et al.  Climate change 2001: The scientific basis. Contribution of Working Group I to the Third Assessment Report of the Intergovernmental Panel on Climate Change , 2002 .

[32]  J. Cory,et al.  Escape from pupal predation as a potential cause of outbreaks of the winter moth, Operophtera brumata , 2002 .

[33]  V. Ossipov,et al.  Interactive effects of leaf maturation and phenolics on consumption and growth of a geometrid moth , 2002 .

[34]  A. Ivashov,et al.  The role of host plant phenology in the development of the oak leafroller moth, Tortrix viridana L. (Lepidoptera: Tortricidae) , 2002 .

[35]  C. Thomas,et al.  The influence of thermal ecology on the distribution of three nymphalid butterflies , 2002 .

[36]  T. M. Bezemer,et al.  Herbivory in global climate change research: direct effects of rising temperature on insect herbivores , 2002 .

[37]  A. Clarke,et al.  Ecology and behavior of first instar larval Lepidoptera. , 2002, Annual review of entomology.

[38]  C. W. Ramm,et al.  Effects of winter temperatures on gypsy moth egg masses in the Great Lakes region of the United States , 2001 .

[39]  T. Tammaru,et al.  Autumnal moth – why autumnal? , 2001 .

[40]  J. Lill SELECTION ON HERBIVORE LIFE‐HISTORY TRAITS BY THE FIRST AND THIRD TROPHIC LEVELS: THE DEVIL AND THE DEEP BLUE SEA REVISITED , 2001, Evolution; international journal of organic evolution.

[41]  P. Brakefield,et al.  Lack of response to artificial selection on the slope of reaction norms for seasonal polyphenism in the butterfly Bicyclus anynana , 2001, Heredity.

[42]  Julie R. Etterson,et al.  Constraint to Adaptive Evolution in Response to Global Warming , 2001, Science.

[43]  Joon-Ho Lee,et al.  Temperature-Dependent Development of Carposina sasakii (Lepidoptera: Carposinidae) and Its Stage Emergence Models , 2001 .

[44]  L. Wilson,et al.  Phenological Synchrony of Eustenopus villosus (Coleoptera: Curculionidae) with Centaurea solstitialis in Idaho , 2001 .

[45]  Marcel E. Visser,et al.  Warmer springs disrupt the synchrony of oak and winter moth phenology , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[46]  J. Hurrell,et al.  The North Atlantic Oscillation , 2001, Science.

[47]  K. Ruohomäki,et al.  HIGH LARVAL PREDATION RATE IN NON-OUTBREAKING POPULATIONS OF A GEOMETRID MOTH , 2001 .

[48]  Massimo Pigliucci,et al.  Phenotypic Plasticity: Beyond Nature and Nurture , 2001 .

[49]  Joon-Ho Lee,et al.  Spring Emergence Pattern of Carposina sasakii (Lepidoptera: Carposinidae) in Apple Orchards in Korea and its Forecasting Models Based on Degree-Days , 2000 .

[50]  D. McCullough A review of factors affecting the population dynamics of jack pine budworm (Choristoneura pinus pinus Freeman) , 2000, Population Ecology.

[51]  T. Tammaru,et al.  Causes of cyclicity of Epirrita autumnata (Lepidoptera, Geometridae): grandiose theory and tedious practice , 2000, Population Ecology.

[52]  Andrew M. Liebhold,et al.  What causes outbreaks of the gypsy moth in North America? , 2000, Population Ecology.

[53]  G. Meehl,et al.  Climate extremes: observations, modeling, and impacts. , 2000, Science.

[54]  A. Menzel,et al.  Trends in phenological phases in Europe between 1951 and 1996 , 2000, International journal of biometeorology.

[55]  D. Simberloff,et al.  SPATIOTEMPORAL VARIATION IN LEAFMINER POPULATION STRUCTURE AND ADAPTATION TO INDIVIDUAL OAK TREES , 2000 .

[56]  David B. Roy,et al.  Phenology of British butterflies and climate change , 2000 .

[57]  Naoto Kamata,et al.  Are population cycles and spatial synchrony a universal characteristic of forest insect populations? : Population dynamics of forest-defoliating insects , 2000 .

[58]  A. Watt,et al.  The effect of phenological asynchrony on population dynamics : analysis of fluctuations of British Macrolepidoptera , 1999 .

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

[60]  P. Merle Egg development and diapause: ecophysiological and genetic basis of phenological polymorphism and adaptation to varied hosts in the green oak tortrix, Tortrix viridana L. (Lepidoptera: Tortricidae). , 1999 .

[61]  T. Klemola,et al.  Different impact of pupal predation on populations of Epirrita autumnata (Lepidoptera; Geometridae) within and outside the outbreak range , 1999 .

[62]  P. Turchin Population regulation : a synthetic view , 1999 .

[63]  A. Nilssen,et al.  Late autumn eclosion in the winter moth Operophtera brumata: compromise of selective forces in life‐cycle timing , 1998 .

[64]  C. Perrins,et al.  Effects of elevated temperature and carbon dioxide on the nutritional quality of leaves of oak (Quercus robur L.) as food for the Winter Moth (Operophtera brumata L.) , 1998 .

[65]  Peter A. Van Zandt,et al.  A Meta‐Analysis of Adaptive Deme Formation in Phytophagous Insect Populations , 1998, The American Naturalist.

[66]  P. Hari,et al.  Effects of dormancy and environmental factors on timing of bud burst in Betula pendula. , 1998, Tree physiology.

[67]  C. Fox,et al.  The adaptive significance of maternal effects. , 1998, Trends in ecology & evolution.

[68]  S. Akimoto Heterogeneous selective pressures on egg‐hatching time and the maintenance of its genetic variance in a Tetraneura gall‐forming aphid , 1998 .

[69]  R. Julkunen‐Tiitto,et al.  HOST-PLANT PREFERENCE OF AN INSECT HERBIVORE MEDIATED BY UV-B AND CO2 IN RELATION TO PLANT SECONDARY METABOLITES , 1998 .

[70]  K. Ozaki Inter‐specific difference in budburst time and its consequences on egg hatch time and survival of the gall‐making adelgid Adelges japonicus (Monzen) (Hom., Adelgidae) , 1998 .

[71]  H. Hänninen,et al.  Freezing exposure releases bud dormancy in Betula pubescens and B. pendula , 1997 .

[72]  E. Kruger,et al.  CO2‐mediated changes in aspen chemistry: effects on gypsy moth performance and susceptibility to virus , 1997 .

[73]  S. Hartley,et al.  Phenology of Winter Moth Feeding on Common Heather: Effects of Source Population and Experimental Manipulation of Hatch Dates , 1997 .

[74]  K. Ruohomäki,et al.  Consequences of defoliation on phenological interaction between Epirrita autumnata and its host plant, Mountain Birch , 1997 .

[75]  T. Backeljau,et al.  Synchronization of hatching date with budburst of individual host trees (Quercus robur) in the winter moth (Operophtera brumata) and its fitness consequences , 1997 .

[76]  J. Good,et al.  Synchronization of larval emergence in winter moth (Operophtera brumata L.) and budburst in pedunculate oak (Quercus robur L.) under simulated climate change , 1996 .

[77]  M. Rossiter,et al.  INCIDENCE AND CONSEQUENCES OF INHERITED ENVIRONMENTAL EFFECTS , 1996 .

[78]  B. Got,et al.  European Corn Borer (Lepidoptera: Pyralidae) Development Time Model , 1996 .

[79]  J. Hill,et al.  Effects of temperature on phenological synchrony and altitudinal distribution of jumping plant lice (Hemiptera: Psylloidea) on dwarf willow (Salix lapponum) in Norway , 1995 .

[80]  F. W. Ravlin,et al.  Further advances toward a model of gypsy moth (Lymantria dispar (L.)) egg phenology: Respiration rates and thermal responsiveness during diapause, and age-dependent developmental rates in postdiapause , 1995 .

[81]  Koen Kramer,et al.  Phenotypic plasticity of the phenology of seven European tree species in relation to climatic warming , 1995 .

[82]  R. Craigen,et al.  Improved Rate Model of Temperature-Dependent Development by Arthropods , 1995 .

[83]  T. Komatsu,et al.  Genetic differentiation as a result of adaptation to the phenologies of individual host trees in the galling aphid Kaltenbachiella japonica , 1995 .

[84]  J. Roland,et al.  Biological Control of the Winter Moth , 1995 .

[85]  M. Montgomery,et al.  Gypsy Moth (Lepidoptera: Lymantriidae) Performance in Relation to Egg Hatch and Feeding Initiation Times , 1994 .

[86]  A. Carroll,et al.  Intratree Variation in Foliage Development Influences the Foraging Strategy of a Caterpillar , 1994 .

[87]  K. Kramer A modelling analysis of the effects of climatic warming on the probability of spring frost damage to tree species in the Netherlands and Germany , 1994 .

[88]  J. Roland After the decline: what maintains low winter moth density after successful biological control? , 1994 .

[89]  Koen Kramer,et al.  Selecting a model to predict the onset of growth of Fagus sylvatica , 1994 .

[90]  A. F. Hunter Gypsy Moth Population Sizes and the Window of Opportunity in Spring , 1993 .

[91]  S. Scheiner Genetics and Evolution of Phenotypic Plasticity , 1993 .

[92]  D. Quiring Rapid change in suitability of white spruce for a specialist herbivore, Zeiraphera canadensis, as a function of leaf age , 1992 .

[93]  A. Watt,et al.  Winter moth on Sitka spruce: synchrony of egg hatch and budburst, and its effect on larval survival , 1991 .

[94]  H. Hänninen Does climatic warming increase the risk of frost damage in northern trees , 1991 .

[95]  G. Whitfield,et al.  Temperature-Dependent Development and Phenology of Pepper Maggots (Diptera: Tephritidae) Associated with Pepper and Horsenettle , 1991 .

[96]  W. Topp,et al.  Synchronisation of pre‐imaginal development and reproductive success in the winter moth, Operophtera brumata L. , 1991 .

[97]  H. Dingle,et al.  Maternal Effects in Insect Life Histories , 1991 .

[98]  M. Hunter Differential susceptibility to variable plant phenology and its role in competition between two insect herbivores on oak , 1990 .

[99]  M. Cannell,et al.  Date of budburst of fifteen tree species in Britain following climatic warming , 1989 .

[100]  Timothy J. Lysyk Stochastic Model of Eastern Spruce Budworm (Lepidoptera: Tortricidae) Phenology on White Spruce and Balsam Fir , 1989 .

[101]  J. Miller,et al.  Effects of temperature on larval eclosion of the winter moth, Operophtera brumata , 1988 .

[102]  Michael J. Crawley,et al.  Individual variation in the phenology of oak trees and its consequences for herbivorous insects , 1988 .

[103]  D. Roach,et al.  MATERNAL EFFECTS IN PLANTS , 1987 .

[104]  L. E. Powell The Hormonal Control of Bud and Seed Dormancy in Woody Plants , 1987 .

[105]  J. Schultz,et al.  Chapter 16 – Insect Population Dynamics and Induction of Plant Resistance: The Testing of Hypotheses , 1987 .

[106]  M. Cannell,et al.  CLIMATIC WARMING, SPRING BUDBURST AND FROST DAMAGE ON TREES , 1986 .

[107]  N. Holliday Maintenance of the phenology of the winter moth (Lepidoptera: Geometridae). , 1985 .

[108]  A. Thomson,et al.  RELATING WEATHER TO OUTBREAKS OF WESTERN SPRUCE BUDWORM, CHORISTONEURA OCCIDENTALIS (LEPIDOPTERA: TORTRICIDAE), IN BRITISH COLUMBIA , 1984, The Canadian Entomologist.

[109]  M. Cannell,et al.  Thermal time, chill days and prediction of budburst in Picea sitchensis , 1983 .

[110]  W. Wint THE ROLE OF ALTERNATIVE HOST-PLANT SPECIES IN THE LIFE OF A POLYPHAGOUS MOTH, OPEROPHTERA BRUMATA (LEPIDOPTERA: GEOMETRIDAE) , 1983 .

[111]  M. Tauber,et al.  Insect Seasonal Cycles: Genetics and Evolution , 1981 .

[112]  P. Sharpe,et al.  Non-linear regression of biological temperature-dependent rate models based on absolute reaction-rate theory. , 1981, Journal of theoretical biology.

[113]  P. Sharpe,et al.  Reaction kinetics of poikilotherm development. , 1977, Journal of theoretical biology.

[114]  S. C. Hoyt,et al.  An Analytic Model for Description of Temperature Dependent Rate Phenomena in Arthropods , 1976 .

[115]  P. Feeny,et al.  Plant apparency and chemical defense , 1976 .

[116]  Risto Sarvas,et al.  Investigations on the annual cycle of development of forest trees. II. Autumn dormancy and winter dormancy , 1974 .

[117]  P. Feeny SEASONAL CHANGES IN OAK LEAF TANNINS AND NUTRIENTS AS A CAUSE OF SPRING FEEDING BY WINTER MOTH CATERPILLARS , 1970 .

[118]  D. G. Embree,et al.  THE DIURNAL AND SEASONAL PATTERN OF HATCHING OF WINTER MOTH EGGS, OPEROPHTERA BRUMATA (GEOMETRIDAE: LEPIDOPTERA) , 1970, The Canadian Entomologist.

[119]  G. Varley,et al.  Population models for the winter moth. , 1968 .

[120]  G. Varley,et al.  Key factors in population studies. , 1960 .