Population Cycles in Forest Lepidoptera Revisited

A quarter century ago, the question was posed of whether a general hypothesis could explain population cycles of forest Lepidoptera. Since then, considerable progress has been made in elucidating mechanisms associated with cyclic dynamics of forest Lepidoptera. Delayed density-related parasitism and reduced fecundity during population peaks are common influences on population dynamics, although why fecundity declines is not understood. The hypothesis that sunspots explain cycles is rejected. The influences of delayed-induced plant defenses on populations are inconsistent, but interactions between plant chemistry, pathogens, and immunity remain rich areas for future study. Population dynamics of forest Lepidoptera can be synchronous over large geographic scales, and repeatable waves of spread of outbreaks occur for some species. Climate warming could modify species distributions and population cycles, but mechanisms have not been elucidated and changes in cyclic dynamics are not generally apparent. Integra...

[1]  A. Allstadt,et al.  Erratum to: Long-term shifts in the cyclicity of outbreaks of a forest-defoliating insect , 2013, Oecologia.

[2]  John P. Buonaccorsi,et al.  Interactions Among Gypsy Moths, White‐footed Mice, and Acorns , 1996 .

[3]  M. Rantala,et al.  Defoliating insect immune defense interacts with induced plant defense during a population outbreak. , 2006, Ecology.

[4]  Alison F. Hunter,et al.  Traits that distinguish outbreaking and nonoutbreaking Macrolepidoptera feeding on northern hardwood trees , 1991 .

[5]  J. Myers,et al.  Is fecundity correlated with resistance to viral disease in the western tent caterpillar? , 1996 .

[6]  A. Fischlin,et al.  The Larch Budmoth in the Alps , 1988 .

[7]  A. Pedersen,et al.  Within and transgenerational immune priming in an insect to a DNA virus , 2011, Proceedings of the Royal Society B: Biological Sciences.

[8]  B. Cooke,et al.  The dynamics of forest tent caterpillar outbreaks across east-central Canada , 2012 .

[9]  A. Berryman What causes population cycles of forest Lepidoptera? , 1996, Trends in ecology & evolution.

[10]  J. Elkinton,et al.  Host Heterogeneity in Susceptibility and Disease Dynamics: Tests of a Mathematical Model , 1997, The American Naturalist.

[11]  Julia Koricheva,et al.  Damage-induced changes in woody plants and their effects on insect herbivore performance: a meta-analysis , 2004 .

[12]  J. Spence,et al.  Responses of natural enemies to experimentally increased populations of the forest tent caterpillar, Malacosoma disstria , 1997 .

[13]  T. Klemola,et al.  Reversed Impacts by Specialist Parasitoids and Generalist Predators May Explain a Phase Lag in Moth Cycles: A Novel Hypothesis and Preliminary Field Tests , 2009 .

[14]  J. Myers EXPERIMENTAL MANIPULATION OF THE PHENOLOGY OF EGG HATCH IN CYCLIC POPULATIONS OF TENT CATERPILLARS , 1992, The Canadian Entomologist.

[15]  M. Rossiter Maternal Effects Hypothesis of Herbivore OutbreakA framework for the inclusion of population-quality variables as central features of herbivore population-dynamics models , 1994 .

[16]  H. Bylund Long-term interactions between the autumnal moth and mountain birch: the roles of resources, competitors, natural enemies, and weather , 1995 .

[17]  J. Cory,et al.  The Ecology and Evolution of Insect Baculoviruses , 2003 .

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

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

[20]  D. Chitty,et al.  The natural selection of self-regulatory behaviour in animal populations , 1967 .

[21]  T. Klemola,et al.  Reduction in size and fecundity of the autumnal moth, Epirrita autumnata, in the increase phase of a population cycle , 2004, Oecologia.

[22]  J. Dushoff,et al.  Host‐Pathogen Interactions, Insect Outbreaks, and Natural Selection for Disease Resistance , 2008, The American Naturalist.

[23]  T. Klemola,et al.  Experimental test of parasitism hypothesis for population cycles of a forest lepidopteran. , 2010, Ecology.

[24]  O. Bjørnstad,et al.  Spatial population dynamics: analyzing patterns and processes of population synchrony. , 1999, Trends in ecology & evolution.

[25]  J. Cory,et al.  Plant-mediated effects in insect-pathogen interactions. , 2006, Trends in ecology & evolution.

[26]  T. Tammaru,et al.  Induced resistance of host tree foliage during and after a natural insect outbreak , 1999 .

[27]  W. Wellington,et al.  Qualitative Changes in Populations in Unstable Environments , 1964, The Canadian Entomologist.

[28]  J. Cory,et al.  The effect of food limitation on immunity factors and disease resistance in the western tent caterpillar , 2011, Oecologia.

[29]  S. Karlsen,et al.  Phase-dependent outbreak dynamics of geometrid moth linked to host plant phenology , 2009, Proceedings of the Royal Society B: Biological Sciences.

[30]  M. Rantala,et al.  Natural host‐plant quality affects immune defence of an insect herbivore , 2007 .

[31]  J. Myers Population fluctuations of the western tent caterpillar in southwestern British Columbia , 2000, Population Ecology.

[32]  Marcel E Visser,et al.  Phenology of forest caterpillars and their host trees: the importance of synchrony. , 2007, Annual review of entomology.

[33]  M. Bonsall,et al.  Invasion and dynamics of covert infection strategies in structured insect–pathogen populations , 2005 .

[34]  W. Baltensweiler Why the larch bud-moth cycle collapsed in the subalpine larch-cembran pine forests in the year 1990 for the first time since 1850 , 1993, Oecologia.

[35]  Population Cycles of the Autumnal Moth in Fennoscandia , 2002 .

[36]  Lev R Ginzburg,et al.  Maternal effects mechanism of population cycling: a formidable competitor to the traditional predator–prey view , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[37]  Andrew M. Liebhold,et al.  Geographic variation in North American gypsy moth cycles: subharmonics, generalist predators, and spatial coupling. , 2010, Ecology.

[38]  J. Cory,et al.  Nucleopolyhedroviruses of forest and western tent caterpillars: cross‐infectivity and evidence for activation of latent virus in high‐density field populations , 2003 .

[39]  N. Colegrave,et al.  Maternal Transfer of Strain-Specific Immunity in an Invertebrate , 2003, Current Biology.

[40]  P. A. P. Moran,et al.  The statistical analysis of the Canadian Lynx cycle. , 1953 .

[41]  M. A. Foster,et al.  Modelling gypsy moth-virus-leaf chemistry interactions: implications of plant quality for pest and pathogen dynamics , 1992 .

[42]  A. Kessler,et al.  Plant‐Induced Responses and Herbivore Population Dynamics , 2012 .

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

[44]  W. Wellington,et al.  Some Maternal Influences on Progeny Quality in the Western Tent Caterpillar, Malacosoma pluviale (Dyar) , 1965, The Canadian Entomologist.

[45]  J. Cory,et al.  Within and between population variation in disease resistance in cyclic populations of western tent caterpillars: a test of the disease defence hypothesis. , 2009, The Journal of animal ecology.

[46]  A. Lynch What Tree‐Ring Reconstruction Tells Us about Conifer Defoliator Outbreaks , 2012 .

[47]  O. Hogstad,et al.  Waves and synchrony in Epirrita autumnata/Operophtera brumata outbreaks. I. Lagged synchrony: regionally, locally and among species. , 2007, The Journal of animal ecology.

[48]  J. Moreau,et al.  Differential expression and costs between maternally and paternally derived immune priming for offspring in an insect. , 2011, The Journal of animal ecology.

[49]  J. Schultz,et al.  Induced plant defenses breached? Phytochemical induction protects an herbivore from disease , 1993, Oecologia.

[50]  Stephen P. Ellner,et al.  POPULATION CYCLES IN THE PINE LOOPER MOTH: DYNAMICAL TESTS OF MECHANISTIC HYPOTHESES , 2005 .

[51]  W. Wellington,et al.  QUALITATIVE CHANGES IN NATURAL POPULATIONS DURING CHANGES IN ABUNDANCE , 1960 .

[52]  T. Klemola,et al.  Local outbreaks of Operophtera brumata and Operophtera fagata cannot be explained by low vulnerability to pupal predation , 2010 .

[53]  N. Yoccoz,et al.  Are population outbreaks in sub-arctic geometrids terminated by larval parasitoids? , 2010, The Journal of animal ecology.

[54]  T. Klemola,et al.  Host plant quality and defence against parasitoids: no relationship between levels of parasitism and a geometrid defoliator immunoassay , 2008 .

[55]  M. Begon,et al.  Disease spread, susceptibility and infection intensity: vicious circles? , 2010, Trends in ecology & evolution.

[56]  Andrew M. Liebhold,et al.  Spatial Synchrony of Insect Outbreaks , 2012 .

[57]  A. Hajek,et al.  Density-dependent resistance of the gypsy moth Lymantria dispar to its nucleopolyhedrovirus, and the consequences for population dynamics , 2007, Oecologia.

[58]  J. Pajares,et al.  Geometrid outbreak waves travel across Europe. , 2013, The Journal of animal ecology.

[59]  W. Baltensweiler,et al.  DYNAMICS OF LARCH BUD MOTH POPULATIONS1,2 , 1977 .

[60]  David W. Williams,et al.  SPATIAL SYNCHRONY IN FOREST INSECT OUTBREAKS: ROLES OF REGIONAL STOCHASTICITY AND DISPERSAL , 2002 .

[61]  T. Klemola,et al.  Geographically partitioned spatial synchrony among cyclic moth populations , 2006 .

[62]  M. Boots,et al.  Group living and investment in immune defence: an interspecific analysis , 2003 .

[63]  Greg Dwyer,et al.  Pathogen‐Driven Outbreaks in Forest Defoliators Revisited: Building Models from Experimental Data , 2000, The American Naturalist.

[64]  L. Rothman IMMEDIATE AND DELAYED EFFECTS OF A VIRAL PATHOGEN AND DENSITY ON TENT CATERPILLAR PERFORMANCE , 1997 .

[65]  M. Boots,et al.  Examining the relationship between hemolymph phenoloxidase and resistance to a DNA virus, Plodia interpunctella granulosis virus (PiGV). , 2010, Journal of insect physiology.

[66]  R. Choquet,et al.  Larch- and pine-feeding host races of the larch bud moth {Zeiraphera diniana) have cyclic and synchronous population fluctuations , 2006 .

[67]  C. Parmesan Ecological and Evolutionary Responses to Recent Climate Change , 2006 .

[68]  Jennifer J. H. Reynolds,et al.  The population dynamical consequences of density-dependent prophylaxis. , 2011, Journal of theoretical biology.

[69]  E. M. Kemp,et al.  Detection of single and mixed covert baculovirus infections in eastern spruce budworm, Choristoneura fumiferana populations. , 2011, Journal of invertebrate pathology.

[70]  R. Knell,et al.  Parental diet has strong transgenerational effects on offspring immunity , 2012 .

[71]  Andrew M. Liebhold,et al.  Circumpolar variation in periodicity and synchrony among gypsy moth populations , 2005 .

[72]  A. Smilanich,et al.  Immune Responses and Their Potential Role in Insect Outbreaks , 2012 .

[73]  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.

[74]  M. Rossiter,et al.  Environmentally-based maternal effects: a hidden force in insect population dynamics? , 1991, Oecologia.

[75]  David F. Rhoades,et al.  Offensive-Defensive Interactions between Herbivores and Plants: Their Relevance in Herbivore Population Dynamics and Ecological Theory , 1985, The American Naturalist.

[76]  Nils Chr. Stenseth,et al.  Climatic warming disrupts recurrent Alpine insect outbreaks , 2010, Proceedings of the National Academy of Sciences.

[77]  A. Agrawal,et al.  Insect outbreaks revisited. , 2012 .

[78]  M. Rantala,et al.  Impact of starvation on immune defense and other life-history traits of an outbreaking geometrid, Epirrita autumnata : a possible causal trigger for the crash phase of population cycle , 2007 .

[79]  O. Tenow,et al.  Waves and synchrony in Epirrita autumnata/Operophtera brumata outbreaks. II. Sunspot activity cannot explain cyclic outbreaks. , 2007, The Journal of animal ecology.

[80]  Camille Parmesan,et al.  Phenological asynchrony between herbivorous insects and their hosts: signal of climate change or pre-existing adaptive strategy? , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[81]  P. Turchin Complex Population Dynamics: A Theoretical/Empirical Synthesis , 2013 .

[82]  Andrew M. Liebhold,et al.  Three centuries of insect outbreaks across the European Alps. , 2009, The New phytologist.

[83]  L. Rothman,et al.  Debilitating Effects of Viral Diseases on Host Lepidoptera , 1996 .

[84]  Veijo Kaitala,et al.  Population dynamic consequences of delayed life-history effects , 2002 .

[85]  É. Bauce,et al.  Does nutrition-related stress carry over to spruce budworm, Choristoneura fumiferana (Lepidoptera: Tortricidae) progeny? , 2002, Bulletin of Entomological Research.

[86]  J. Elkinton,et al.  EFFECTS OF SYNCHRONY WITH HOST PLANT ON POPULATIONS OF A SPRING-FEEDING LEPIDOPTERAN , 2000 .

[87]  J. Roland,et al.  Generalist predation on forest tent caterpillar varies with forest stand composition: an experimental study across multiple life stages , 2012 .

[88]  J. Myers,et al.  SYNCHRONY IN OUTBREAKS OF FOREST LEPIDOPTERA: A POSSIBLE EXAMPLE OF THE MORAN EFFECT , 1998 .

[89]  B. Kendall,et al.  DYNAMICAL EFFECTS OF PLANT QUALITY AND PARASITISM ON POPULATION CYCLES OF LARCH BUDMOTH , 2003 .

[90]  T. Klemola,et al.  Fecundity of the autumnal moth depends on pooled geometrid abundance without a time lag: implications for cyclic population dynamics. , 2008, The Journal of animal ecology.

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

[92]  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.

[93]  J. Cory,et al.  Life‐history consequences and disease resistance of western tent caterpillars in response to localised, herbivore‐induced changes in alder leaf quality , 2013 .

[94]  J. Régnière,et al.  The fine‐scale population dynamics of spruce budworm: survival of early instars related to forest condition , 2008 .

[95]  Greg Dwyer,et al.  The combined effects of pathogens and predators on insect outbreaks , 2004, Nature.

[96]  Andrew M. Liebhold,et al.  Effects of alternative prey on predation by small mammals on gypsy moth pupae , 2004, Population Ecology.

[97]  K. Wilson,et al.  Density‐dependent prophylaxis: evidence from Lepidoptera–baculovirus interactions? , 1998 .

[98]  P. Schmid-Hempel,et al.  Strain-specific priming of resistance in the red flour beetle, Tribolium castaneum , 2009, Proceedings of the Royal Society B: Biological Sciences.

[99]  Andrew M. Liebhold,et al.  POPULATION DYNAMICS OF GYPSY MOTH IN NORTH AMERICA , 1990 .

[100]  Greg Dwyer,et al.  Induced plant defenses, host–pathogen interactions, and forest insect outbreaks , 2013, Proceedings of the National Academy of Sciences.

[101]  M. Saurer,et al.  Summer temperature dependency of larch budmoth outbreaks revealed by Alpine tree-ring isotope chronologies , 2009, Oecologia.

[102]  J. Myers,et al.  Can a General Hypothesis Explain Population Cycles of Forest Lepidoptera , 1988 .

[103]  J. Elkinton,et al.  Using simple models to predict virus epizootics in gypsy moth populations , 1993 .

[104]  J. Elkinton,et al.  MATERNAL EFFECTS IN GYPSY MOTH: ONLY SEX RATIO VARIES WITH POPULATION DENSITY , 1998 .

[105]  Andrew M. Liebhold,et al.  Waves of Larch Budmoth Outbreaks in the European Alps , 2002, Science.

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

[107]  B. Elderd,et al.  Pathogen Persistence in the Environment and Insect-Baculovirus Interactions: Disease-Density Thresholds, Epidemic Burnout, and Insect Outbreaks , 2012, The American Naturalist.

[108]  Alan A. Berryman,et al.  Population cycles : the case for trophic interactions , 2002 .

[109]  D. Heckel,et al.  Dietary-dependent trans-generational immune priming in an insect herbivore , 2009, Proceedings of the Royal Society B: Biological Sciences.

[110]  Marcel E Visser,et al.  Climate change and unequal phenological changes across four trophic levels: constraints or adaptations? , 2009, The Journal of animal ecology.