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ES44CH26-Myers ARI 28 October 2013 ANNUAL REVIEWS Further 15:17 Annu. Rev. Ecol. Evol. Syst. 2013.44:565-592. Downloaded from www.annualreviews.org by Lomonosov Moscow State University on 11/28/13. For personal use only. Click here for quick links to Annual Reviews content online, including: • Other articles in this volume • Top cited articles • Top downloaded articles • Our comprehensive search Population Cycles in Forest Lepidoptera Revisited Judith H. Myers1 and Jenny S. Cory2 1 Department of Zoology, and Biodiversity Research Center, University of British Columbia, Vancouver, BC, Canada V6T 1Z4; email: [email protected] 2 Department of Biological Sciences, Simon Fraser University, Burnaby, BC, Canada V5A 1S6; email: [email protected] Annu. Rev. Ecol. Evol. Syst. 2013. 44:565–92 Keywords First published online as a Review in Advance on October 18, 2013 cyclic dynamics, synchrony, traveling waves, climate change, parasitism, pathogens, immunity The Annual Review of Ecology, Evolution, and Systematics is online at ecolsys.annualreviews.org This article’s doi: 10.1146/annurev-ecolsys-110512-135858 c 2013 by Annual Reviews. Copyright All rights reserved Abstract 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. Integration of top-down and bottom-up influences on cyclic dynamics and quantification of dispersal are necessary for progress in understanding patterns of insect outbreaks. 565 ES44CH26-Myers ARI 28 October 2013 15:17 INTRODUCTION Annu. Rev. Ecol. Evol. Syst. 2013.44:565-592. Downloaded from www.annualreviews.org by Lomonosov Moscow State University on 11/28/13. For personal use only. All animal populations fluctuate over time and space. For a subset of species, populations oscillate on a regular basis. In the relatively early days of the science of ecology, the oscillations of populations challenged the broadly held “equilibrium view” of population regulation. The question of whether population cycles are determined by biotic or abiotic or by intrinsic or extrinsic factors has been hotly debated ever since Elton (1927). Initially, most research on insect cycles was carried out by field ecologists, who monitored populations over many generations. Their focus was primarily on the population trends and the causes of mortality. Myers (1988) reviewed the hypotheses that were proposed to explain cyclic population dynamics, including climatic release, bottom-up influences of food limitation, induced plant defenses or changes in food quality, top-down influences of pathogens, parasitoids or predators, and intrinsic changes in quality that are passed on to offspring by their mothers. She posed the question of whether a general hypothesis could explain population cycles of forest Lepidoptera and concluded that measuring mortality alone is not sufficient for understanding cyclic dynamics. Information on reproduction and dispersal is also needed. She also suggested that the importance of pathogens might have been generally overlooked. Twenty-five years later, we revisit the question of generality by reviewing recent work and ask, “What are the common characteristics of forest Lepidoptera populations that might explain their cyclic dynamics?” Population ecologists have a tendency to emphasize the mystery of population cycles perhaps to rationalize what they do. Without a doubt, the boom and bust dynamics of some species are fascinating not only to ecologists but also nonecologists who see widespread defoliation and are faced with periodic rains of frass or writhing masses of caterpillars. But the cyclic dynamics of these populations are captivating in many regards. For example, given the long-term data sets that are available, the influences of changing environmental conditions on population cycles can now be identified. Currently for all ecological systems, climate change has the potential to dramatically modify the patterns of population dynamics and the associations among species (Parmesan 2006). The elegant symmetry in temporal population data of cyclic species is also of interest to theoretical ecologists. Can models be developed that create cyclic dynamics? Can they mimic the observed patterns of synchrony and spread? Much has happened since the last review by Myers (1988); data sets have become longer, techniques for remote sensing have become more sophisticated, new and accessible statistical techniques have been developed, and more experimental results to investigate potential mechanisms have accumulated. In order to assess whether we are approaching a better general understanding of the underlying processes regulating population dynamics in forest Lepidoptera, we 1. review classic examples of population cycles to describe differences and similarities in patterns of density change, parasitism, and fecundity; 2. evaluate some of the hypotheses proposed to explain the dynamics of cyclic populations in the light of recent data; 3. consider the advances in elucidating patterns of synchrony among populations and waves of outbreak spread and how they might be influenced by climate change and phenology; 4. suggest new directions for future studies to expand our understanding of potential mechanisms underpinning cyclic population dynamics at different scales. CONDITIONS FOR CYCLIC DYNAMICS Three factors are required for cyclic population dynamics: (a) sufficiently high fecundity and/or survival to allow the population to increase by three to six orders of magnitude during the four 566 Myers · Cory ES44CH26-Myers ARI 100 a 1,000 80 100 60 10 40 1 20 0.1 1986 1990 1994 1998 2002 2006 2010 10,000 260 b Population trend (number of tents) Population trend Percent infected Percent parasitized Mean eggs 0 2014 1,000 240 100 220 10 200 1 180 0.1 1986 1990 1994 1998 2002 2006 2010 Mean eggs per mass (N+1) Annu. Rev. Ecol. Evol. Syst. 2013.44:565-592. Downloaded from www.annualreviews.org by Lomonosov Moscow State University on 11/28/13. For personal use only. 15:17 Percent parasitized or families infected Population trend (number of tents) 10,000 28 October 2013 160 2014 Year Figure 1 (a) Population trend (shaded area), percent parasitized (red dashed line), and percent families of western tent caterpillars infected by nucleopolyhedrovirus (blue solid line) on Galiano Island in southwestern British Columbia. (b) Mean eggs per egg mass for moths in the year indicated. These will give rise to the population in the next generation. ( J. H. Myers and J. S. Cory, unpublished). or five generations of the increase phase, (b) density-related, increased mortality factor(s) that initiate the decline at peak density, and (c) a delayed density-related mechanism(s) that prolongs the population decline. The factors that initiate the population decline need not be the same as those that prolong the decline. Examples of Population Cycles and Population Trends To illustrate the cyclic dynamics of forest Lepidoptera, we have chosen three species that have been studied for a sufficiently long period of time for patterns to be clear, and for which data on population density and parasitism or disease have been collected (Figures 1–3). These are the western tent caterpillar (WTC), Malacosoma californicum pluviale (Lasiocampidae) (Wellington 1960, Myers 2000, Cory & Myers 2009); the autumnal moth (AM), Epirrita autumnata (Geometridae) (Bylund 1995, Ruohomäki et al. 2000, Tanhuanpää et al. 2002, Tenow et al. 2007); and the larch budmoth (LBM), Zeiraphera diniana (Tortricidae) (Baltensweiler & Fischlin 1988, Dormont et al. 2006). Each of these studies has measured insect abundance directly, rather than having merely monitored patterns of defoliation, and this allows better illustration and understanding of their dynamics. Although overwintering as eggs and laying eggs in masses are traits www.annualreviews.org • Population Cycles in Lepidoptera 567 ES44CH26-Myers ARI 28 October 2013 15:17 100 1,000 80 100 10 60 1 40 0.1 0.01 Percent parasitized or leaf length (mm) Population trend (larch budmoth / kg foliage) 10,000 Population trend Percent parasitized Leaf quality 20 1945 1950 1955 1960 1965 1970 1975 1980 1985 1990 Annu. Rev. Ecol. Evol. Syst. 2013.44:565-592. Downloaded from www.annualreviews.org by Lomonosov Moscow State University on 11/28/13. For personal use only. Year Figure 2 Population trend (shaded ) and percent parasitized (red dashed line) with change in leaf quality, indicated by needle length of subalpine larch for larch budmoth in the Engadine Valley in the Swiss Alps. Data collected by W. Baltensweiler and made available by P. Turchin (http://www.eeb.uconn.edu/people/turchin/ NLTSM.htm). that occur more commonly among outbreak species of forest Macrolepidoptera (Hunter 1991), of these three species, only tent caterpillars lay eggs in masses and have gregarious larvae. All three of the species have a single generation per year, overwinter as eggs, and have peaks of population density every 6 to 11 years, with most outbreaks occurring every 8 to 10 years. In addition, the patterns of the population cycles are comparable in that the duration of the increase and peak phases tends to be more variable than that of the decline phase, which usually occurs over two generations. This pattern is common in other cyclic species of forest Lepidoptera (Myers 1988). Patterns of Parasitism and Disease The impact of larval parasitoids has been monitored for all three focal species. The general trend is for parasitism to reach high levels at or just after the peak of population density (Figures 1a–3a) and remain high for one to two generations. According to models, parasitism explains a significant portion of the density variation in the LBM (Turchin et al. 2003) and in the AM (Tanhuanpää et al. 2002). Parasitism acts in a delayed density-dependent manner. Density-related infection by a baculovirus (nucleopolyhedrovirus, NPV) initiates the population declines of the WTC (Figure 1a). Baculovirus epizootics in forest Lepidoptera occur most commonly in species in the families Lymantriidae [gypsy moth (GM), Lymantria dispar, and tussock moths, Orygia spp.] and Lasiocampidae (tent caterpillars) (Cory & Myers 2003). The role of pathogens is less clear for the Geometridae and Tortricidae. Granulovirus infection (another type of baculovirus) did occur in the LBM in the peak years of 1955 and 1964 (Baltensweiler & Fischlin 1988). Tenow (1972) found high numbers of AM larvae killed by a cypovirus (CPV) in the 1955 and 1965–1966 outbreaks, and NPV infection was observed in AM larvae in 2003–2004 and again in 2012 by Helena Bylund (personal communication). The occurrence of disease has not been monitored in a consistent manner in LBM or AM. Patterns of Fecundity and Surrogates of Fecundity In addition to the changes in mortality of cyclic forest Lepidoptera, fecundity, moth size, and fitness also vary with population density for these three species. Changes in fecundity are best 568 Myers · Cory ES44CH26-Myers ARI 28 October 2013 100 100 80 10 60 1 40 0.1 20 0.01 0.001 1954 Population trend, autumnal moth Population trend, winter moth Percent parasitized Moth size 0 1959 1964 1984 1989 1994 1999 Year b Moth size 2.5 Population trend (larval density index) 1,000 2.4 100 2.3 2.2 10 2.1 1 1998 2000 2002 2004 2006 Moth size (femur length, mm) Annu. Rev. Ecol. Evol. Syst. 2013.44:565-592. Downloaded from www.annualreviews.org by Lomonosov Moscow State University on 11/28/13. For personal use only. Parasitized 1,000 Percent parasitized Population trend (mean number of larvae per branch) a 15:17 2.0 Year Figure 3 (a) Population trend (shaded ) and percent parasitized (red dashed line) for autumnal moth based on two sites in the Abisko Valley, Sweden. Data provided by O. Tenow and H. Bylund. (b) Population trend for autumnal moth (shaded ) and that pooled with four generations of winter moth (thick line) in Hana, northern Norway. Moth size is reflected by the femur length ( green dashed line). Note the continued high density of winter moth after the autumnal moth declined. Data provided by T. Klemola (Klemola et al. 2008). described for the WTC. Each female moth lays all of her eggs in a single egg mass that remains on the branch and can be collected and counted after the eggs hatch. For the WTC, fecundity peaks just before or at peak density and then declines for several consecutive generations (Figure 1b) (Myers 2000). Three hypotheses that have been proposed to explain the decline in fecundity of the WTC are (a) food limitation, (b) sublethal infection of late instar larvae or the costs of fighting infection (Rothman & Myers 1996a), or (c) a cost of selection for resistance to viral infection. Direct evidence from field experiments relates both larval density and viral exposure to the reduced egg mass sizes of surviving moths and the pupal weights (a surrogate for fecundity) of their female offspring (Rothman 1997). Evidence does not support the third hypothesis because larvae from smaller egg masses are not more resistant to viral infection (Rothman & Myers 1996b, Cory & Myers 2009). For field populations of WTCs, moth fecundity explains approximately 30% of the variation in the rate of population increase between generations ( J. H. Myers and J. S. Cory, unpublished data). www.annualreviews.org • Population Cycles in Lepidoptera 569 ARI 28 October 2013 15:17 Indicators of fecundity change for the LBM are indirect. Defoliation by high densities of larvae reduces the length of larch needles in subsequent generations (Figure 2), and related to this are increased fiber content and reduced nutritional quality. Based on laboratory studies by Benz, who fed larvae needles of different lengths, Turchin (2003) calculated that needle length explained 86% of the variation in LBM fitness measured as survival and fecundity. Baltensweiler et al. (1977) reported that fecundity declines by 75% to 85% in the year following defoliation. Thus, like the WTC, fecundity of the LBM is reduced during the population decline. The sizes of moths and pupae are well correlated to fecundity (Kaitaniemi et al. 1999). Considerable experimental work has been carried out in this system to relate moth fecundity and fitness to larval feeding damage to host trees. Pupae resulting from larvae reared in bags on trees over a period of outbreak density were larger in the peak than in two subsequent years (T. Klemola et al. 2004). Pupal mass and moth size of the AM were weakly related to defoliation in the previous generation (Kaitaniemi et al. 1999). T. Klemola et al. (2008) showed that adult moths were smaller late in the peak but increased to moderate size again as the decline progressed (Figure 3b). An interesting twist is that, in addition to outbreaks of the AM, the winter moth (WM), Operophtera brumata, also feeds on the same trees in this area and typically reaches peak density two years after the AM (Tenow et al. 2007). The decline in AM size and fecundity at peak densities is unlikely to be explained by reduced host-tree quality as the host quality was still sufficient to support outbreak densities of the WM. Kaitaniemi et al. (1999) concluded that the reduction of fecundity at peak density of the AM is insufficient to explain the population decline without other factors. Annu. Rev. Ecol. Evol. Syst. 2013.44:565-592. Downloaded from www.annualreviews.org by Lomonosov Moscow State University on 11/28/13. For personal use only. ES44CH26-Myers Summary The similarities in population trends shown in Figures 1–3, and the characteristics associated with the dynamics of these three well-studied species summarized in Figure 4, occur even though the species are in different families, live in different habitats, and have different host trees and parasitoid complexes. In all of these examples, crowding at peak density reduces moth size and thus fecundity, and this can persist over several generations of population decline. It is unlikely Feeding damage Increased infection (WTC) Reduced fecundity Reduced larval survival Negative R Increased parasitism Increased dispersal? High density Positive R Low density Increased fecundity Improved survival Low infection (WTC) Reduced parasitism Figure 4 Factors related to the rate of population increase R (density at Nt +1 /density at Nt ) of cyclic populations of forest Lepidoptera. Abbreviation: WTC, western tent caterpillar. 570 Myers · Cory Annu. Rev. Ecol. Evol. Syst. 2013.44:565-592. Downloaded from www.annualreviews.org by Lomonosov Moscow State University on 11/28/13. For personal use only. ES44CH26-Myers ARI 28 October 2013 15:17 that the levels of reduced fecundity are sufficient to create cyclic dynamics without the influence of increased mortality from parasitism that also occurs for several generations during the population declines (Figures 1–3). This is an area that deserves more exploration with models such as those of Turchin et al. (2003) and Kendall et al. (2005) that incorporate both parasitism and moth quality and conclude that both are important. In addition, although the population cycles of eastern spruce budworm, Choristoneura fumiferana, differ from the three species described above in that outbreaks are more prolonged with defoliation lasting for 10 years or more, Régnière & Nealis (2008) propose that the impact of larval defoliation on tree condition reduces the survival of dispersing early-instar larvae. They attribute the cyclic population dynamics to reduced early larval survival exacerbated by other factors, including maternal fecundity, infection by the microsporidian Nosema fumiferanae, and weather influences, as well as density-related mortality from natural enemies. It is likely that both top-down and bottom-up processes are involved in cyclic population dynamics of forest Lepidoptera. TESTING HYPOTHESES Since 1988 considerable information has accumulated that allows a more critical look at some of the hypotheses that have been formulated to explain cyclic population dynamics of forest Lepidoptera and to suggest those that look most promising for future research. The complexity of these cyclic populations and the variation of the habitats and communities in which they exist make it difficult to reject any hypothesis definitively; however, it is becoming clear that no one hypothesis will explain all population cycles in forest Lepidoptera, and combinations of several factors will form the most likely explanation. The Role of Parasitoids in Cyclic Dynamics Alan Berryman (1996, 2002) has been the strongest proponent of the importance of parasitoids as the driving force in population cycles. Certainly parasitism is a universal mortality factor for forest Lepidoptera and, as shown in Figures 1–3, it can reach very high levels following peak population densities of the hosts. Not only that, but parasitism generally remains high for several generations following host decline and thus fulfills the delayed density-dependent criteria for cyclic dynamics. Carrying out field experiments on the role of parasitoids is difficult, but this has been accomplished recently for the AM (Klemola et al. 2010). Over four years of high and declining AM populations in northern Finland, the exclusion of parasitoids allowed continued high host densities as compared to natural populations or those in exclosures permeable to parasitoids. In contrast, parasitism of larvae was found to be weakly correlated to population growth of the AM and WM over an elevational gradient on a Norwegian coastal island (Schott et al. 2010). Although some of the geographical variation in population growth rate was related to parasitism, temporal variation in the rate of population growth was not. Larval densities at these sites were lower than the outbreak densities of continental populations, and defoliation did not occur. Cyclic dynamics were most apparent at high elevation sites only. It is possible that these populations are influenced by immigration of moths or ballooning larvae from the traveling wave of outbreaks that occur in continental populations (see below). In comparison, an analysis of Bylund’s (1995) and subsequent data on a continental population of the AM (illustrated in Figure 3a) shows a significant negative relationship between R = log (n + 1/n) and parasitism (r2 = 0.23, p < 0.02). With a very simple model based on these data, Tanhuanpää et al. (2002) concluded that parasitism could explain the cycles of the AM. Klemola et al. (2009) compared parasitism and predation of the AM and the WM over a population outbreak and found that increased parasitism occurred www.annualreviews.org • Population Cycles in Lepidoptera 571 ES44CH26-Myers ARI 28 October 2013 15:17 late in the peak of the AM but not of the WM. For the latter, predation of pupae was higher. In addition, the models of the LBM (Turchin et al. 2003) and of the pine looper, Bupalus piniarus (Kendall et al. 2005), provide strong support for the parasitoid hypothesis, although both of these analyses also found that factors associated with food quality and fecundity strongly contributed to the population dynamics. We conclude that though it is difficult, time consuming, and expensive, more work should focus on parasitism, including investigations of the host ranges and the geographical distributions of parasitoids. Questions such as whether parasitoids are maintained by alternate hosts, whether they move readily among populations and can synchronize host populations, and how egg and pupal parasitoids contribute to host dynamics deserve further study. Annu. Rev. Ecol. Evol. Syst. 2013.44:565-592. Downloaded from www.annualreviews.org by Lomonosov Moscow State University on 11/28/13. For personal use only. The Role of Predation at Low Prey Densities As mentioned above, Klemola et al. (2009) found that predation on WM pupae was greater than that on AM pupae, although in other field experiments differential predation was not statistically significant (Heisswolf et al. 2010). Klemola et al. (2009) suggested that pupal predation could prolong the lag phase for the WM as compared with the AM and cause the cycles of the two species to be out of phase by one to two generations. Previously, Roland (1994) showed that the initial decline of the WM introduced to Canada was associated with high parasitism by the biological control agent, Cyzenis albicans, but that generalist ground predators, primarily polyphagous beetles, regulated populations at lower densities. In a similar situation, deer mice, Peromyscus maniculatus, feed on pupae and larvae of GMs, and Elkinton et al. (1996) suggested that deer mice could play a role in maintaining low GM density. This situation is particularly interesting because it involves three trophic levels: the GM prey, the predacious deer mice, and oak trees that provide leaves for GM larvae and acorns for the mice. Although years of high acorn production were correlated to increased mouse abundance, and thus predation on GM, further study showed that GM pupae and larvae were not as attractive to deer mice as were alternative prey items and that predation was closer to a type 2 functional response than to a type 3 functional response that could prolong the low density of GMs. Elkinton et al. (2004) concluded that predation by small mammals was unlikely to stabilize low-density populations of GMs. Models of GM populations that included mortality from a generalist predator or parasitoid following a type 3 rather than a type 2 functional response and a specialist virus resulted in more irregular lengths of cycles but not long periods of low density (Dwyer et al. 2004). Further analysis of the total 86 years of GM defoliation in the northeastern US by Allstadt et al. (2013) shows periods of noncyclical and cyclical dynamics with harmonic oscillations of 4–5 and 8–10 years during the latter. They suggest that predators create extended periods of noncyclical dynamics of GMs. Unfortunately there are no actual long-term population data on GMs, small mammals, and viral infection to test the various models, and thus conclusions remain speculative. The contradictory results of these studies make conclusions impossible. Bird predation is common for low-density populations of the forest tent caterpillar (FTC), Malacosoma disstria, in aspen and mixed boreal forests in Alberta, Canada (Parry et al. 2003). Generalist predation on FTC was higher in aspen than in mixed-wood stands, and Nixon & Roland (2012) suggest that this may cause FTC populations to be slower to reach outbreak levels in aspen stands. This relationship has not yet been tested. To conclude, predators have not received as much empirical study as parasitoids in relation to cyclic population dynamics, partially because they are difficult to study and require elaborate designs to manipulate. Also they are generalists and not dependent on the moths. Predation from spiders, beetles, small mammals, and birds remains a black box in most population studies. Support 572 Myers · Cory ES44CH26-Myers ARI 28 October 2013 15:17 for the hypothesis that generalist predators maintain a low-density lag phase in the cyclic dynamics of forest Lepidoptera is weak. Annu. Rev. Ecol. Evol. Syst. 2013.44:565-592. Downloaded from www.annualreviews.org by Lomonosov Moscow State University on 11/28/13. For personal use only. Future direction: empirical studies of predation. Further experimental work to elucidate the impact of generalist predators in low-density populations of forest Lepidoptera is required to determine predators’ roles in the cyclic population dynamics of forest Lepidoptera. This is of particular interest to the interactions between sympatric populations of the AM and the WM. Future direction: testing the predictions of models. Predictions arising from the numerous models of the interactions among GM populations, predators and viral disease should be tested with field data and reasons for contradictory conclusions among studies should be recognized and discussed. It should be imperative for future modeling studies to explicitly state testable predictions. Pathogen Impact in Cyclic Populations The main group of pathogens associated with forest Lepidoptera is baculoviruses. The symptoms of infected larvae are very distinctive and can result in spectacular epizootics in high-density populations and are often associated with population declines. The population dynamics of the WTC and the GM are strongly influenced by NPV infection (Myers 2000, Cory & Myers 2009, Dwyer & Elkinton 1993). In the buildup to an epizootic, NPV is spread horizontally following the death of an infected larva. NPV infection clearly responds to rising host density and is strongly implicated in the population crash in the WTC, with peak mortality and peak density coinciding (Figure 1). In addition, baculoviruses can produce delayed influences through sublethal effects (Rothman & Myers 1996a) or potentially, although less likely, through costs of resistance (discussed above). Dwyer and colleagues have produced a detailed series of mathematical models supported by manipulative lab and field experiments to describe the interaction between the GM and NPV (Dwyer et al. 1997, 2000; Elderd et al. 2008). These models focus in particular on heterogeneity in infection risk associated with resistance. The model outputs have been compared to patterns of defoliation rather than to actual data on GM populations and infection and thus are difficult to interpret particularly as dynamics change over time (Allstadt et al. 2013). One of the key issues with the NPVs of the WTC and the GM is that they are both host-specific and the host is univoltine. Thus the virus has to persist from one year to the next and across several years when host populations are low, at least in the WTC (Figure 1). In the absence of alternative hosts, the only way for the pathogen to persist is via either environmental persistence or vertical transmission from parents to offspring. Fuller et al. (2012) believe that environmental persistence is sufficient to maintain the pathogen in GM populations. However, with the use of polymerase chain reaction (PCR) to amplify small quantities of virus DNA or RNA from adult moths, it is clear that baculovirus infections can persist in adult Lepidoptera. For example, 70% of adult eastern spruce budworm, Choristoneura fumiferana, individuals sampled were positive for NPV DNA (Kemp et al. 2011). Presence of this DNA is not usually expressed as overt disease in the offspring generation and is regarded as a covert infection. Investigation of the WTC has also demonstrated the presence of covert NPV infection, the level of which appears to fluctuate with host population density; i.e., it cycles ( J. S. Cory and J. H. Myers, unpublished data). To have a significant impact on population dynamics, covert virus would need to convert at some rate to an overt infection that could be horizontally transmitted through the host population www.annualreviews.org • Population Cycles in Lepidoptera 573 ES44CH26-Myers ARI 28 October 2013 15:17 (Bonsall et al. 2005). Although a variety of mechanisms have been suggested as triggers, none have been consistently found. Cross infection of FTCs from high-density populations with WTC virus resulted in the apparent expression of a covert FTC NPV (Cooper et al. 2003). This suggests that such conversions can occur when stimulated by a nonhost virus. Also, spontaneous overt infection does occur at a low level (0.5% to 10% of egg masses or larvae) in larvae hatching from surface-sterilized eggs transferred to trees not previously attacked by WTCs or in laboratory-reared larvae ( J. S. Cory and J. H. Myers, unpublished data). Annu. Rev. Ecol. Evol. Syst. 2013.44:565-592. Downloaded from www.annualreviews.org by Lomonosov Moscow State University on 11/28/13. For personal use only. Future direction: virus persistence through covert infection. Although it seems quite feasible that different mechanisms play roles in host species with differing ecologies, a clear understanding of the relative importance of environmental versus vertical routes of virus persistence at differing host densities is needed to explain insect-pathogen dynamics fully. The transition from vertically transmitted covert infection to lethal, horizontally transmitted, overt infection is of particular relevance to field populations and of interest to theoretical and evolutionary ecologists. Future direction: probing pathogen communities. The current lack of evidence for widespread pathogen infection in other cyclic species might indicate that this is not a general mechanism driving population dynamics of forest Lepidoptera. However, only the more obvious pathogen infections (like NPVs) tend to be identified, and insects are likely to be carrying a range of pathogens that may have chronic effects and be less readily identified visually. For example, as mentioned above, viral infections, particularly cypovirus infections, have been observed in the LBM, the AM, and the WM, and microsporidian infection is common in eastern spruce budworm. With PCR and second-generation sequencing, it is now possible to identify the pathogen community present in host populations. This could be an important new way to describe the quality of insects in different populations or at different stages of the cycle. The Sunspot Hypothesis Ecologists have long been interested in patterns of biological cycles among species (Huntington 1931). In a summary of population outbreaks of forest Lepidoptera, Myers (1998) observed an apparent clustering of peak populations in some years. This caused her to look for a global cuing mechanism for population outbreaks. Sunspots seemed a possible explanation as troughs of sunspots are associated with cooler temperatures. Ruohomäki et al. (2000) also noted the correspondence between sunspot cycles and AM population cycles. Selås et al. (2004) reported a negative relationship between sunspot activity and populations of AM and WM in central and southern Norway. They proposed a rather complex mechanism based on the ozone layer, and the trade-off between the production of UV-B protective pigments and insect defenses. Haukioja (2005) expanded on this idea, suggesting that high UV-B could trigger the octadecanoid pathway, which could increase the immunocompetence of larvae and thus protect them against disease and parasitism and allow the population outbreaks. The flaw in the original suggestion of a pattern between insect outbreaks, with normally an 8- to 10-year periodicity, and sunspots with an 11-year periodicity is that these two sequences will run in and out of phase over time. This is exactly what was revealed by sufficiently long sets of data. Nilssen et al. (2007) compared a 114-year data set showing the periodicity of AM outbreaks and the sunspot record and found that the two sequences do run in and out of phase. Thus, even though sunspot numbers might influence temperature and plant exposure to UV-B, they cannot be considered to be a long-term driver of population cycles. The sunspot hypothesis should be rejected. 574 Myers · Cory ES44CH26-Myers ARI 28 October 2013 15:17 Annu. Rev. Ecol. Evol. Syst. 2013.44:565-592. Downloaded from www.annualreviews.org by Lomonosov Moscow State University on 11/28/13. For personal use only. Induced Plant Defenses The discovery that plant secondary compounds change following herbivore damage brought the idea that this could drive the population cycles of forest Lepidoptera (Rhoades 1985, Haukioja & Neuvonen 1987). Effects of the induced secondary compounds of trees can act rapidly in the current generation of larvae as population density rises and defoliation increases, and they can also be passed on through changes in foliage quality in the years following an outbreak. This creates delayed effects that can extend into the population decline, thereby providing a mechanism to promote cycles. The amount of work done on this hypothesis is extensive, and the results are contradictory (reviewed by Nykänen & Koricheva 2004, Kessler et al. 2012). Although there is clear evidence that changes in plant quality as a result of damage can alter growth rate, survival, and fecundity of moths, links to changing population density in the field have not been found. Much of the work in this area has been done with the AM system. Haukioja (2005), who was one of the initial proponents of the potentially important role of induced plant defenses in insect population dynamics, has concluded that “delayed inducible production of secondary compounds does not seem to explain cyclic fluctuations in population density” for the AM (p. 313). Although induced effects alone may not appear to have an impact, they could combine with other factors, such as through their effect on immunity and interactions with natural enemies (see below). Induced plant defenses are likely to vary among host tree species and conditions and thus are unlikely to be a general mechanism causing cyclic population dynamics. We conclude that by itself, the induced plant defense hypothesis is not supported even though changes in plant chemistry following insect attack might interact with insect diseases, parasitoids, or larval growth in complex ways (Sarfraz et al. 2013). Future direction: host-quality influences on insect phenotypes in the field. Given the variation in response to different chemistries, further research in this area should focus on the overall impacts on insect phenotype in field populations, including the impacts on life-history traits, behavior, and selection at different phases of the population cycle. Future direction: projections from individual phenotypes to population dynamics. Projections of the influences of induced plant changes on individual insects to population dynamics should be done with caution. The variable conditions in the field such as different host plants and levels of attack influence how individual impacts scale up to population dynamics. Insect Quality and Immunocompetence One area that has attracted increasing attention in recent years is the role of insect quality or condition and, in particular, changes in insect immunocompetence. This returns us to the ideas of Wellington (1960) and Chitty (1971) and moves the focus back to the impact of broader changes in insect quality rather than identifying the individual factors that might modify it. The basic idea is that changes in food quality or quantity could modify both insect condition and susceptibility to disease or parasitism through influences on immunocompetence at different points of the population cycle (Haukioja 2005, Shlichta & Smilanich 2012). Immune response and natural enemy protection. A particular focus has been on population increase and whether an enhanced immune response could allow individuals to escape their natural enemies (Haukioja 2005). Considerable experimental work has been done on the pupal parasitoids of the AM to test this relationship. Variation in tree quality (assessed by insect growth rate) and plant chemistry can alter pupal immunocompetence. For example, changes in foliage quality the www.annualreviews.org • Population Cycles in Lepidoptera 575 ARI 28 October 2013 15:17 year following defoliation resulted in an increased ability of pupae to encapsulate a foreign object used as a surrogate for parasitoid eggs (Kapari et al. 2006). However, observed encapsulation in the laboratory was low, and no link could be found between changes in immunity and pupal parasitism in the field. The idea that changes in immunocompetence either drive or modulate population cycles in this system is not supported (N. Klemola et al. 2007, 2008). Similarly the impact of induced plant chemicals on insect pathogens is variable. Many entomopathogens are affected by the insect host plant (Cory & Hoover 2006). However, whether these changes are brought about through a direct effect of host-plant secondary chemicals on the pathogen itself or altered immunity is less clear. As an example, in the GM the hydrolyzable tannins induced by feeding on oak reduced NPV mortality in laboratory studies and led to the suggestion that induction actually protects the insects (Hunter & Schultz 1993). This was predicted to destabilize GM populations at intermediate tannin levels (Foster et al. 1992). Transmission of virus in the field is more complex and is related to insect behavior, variation in the dose ingested, changes in insect susceptibility related to larval stage, and the breakdown in virus activity. A recent study revisited the induction hypothesis and focused on the effect of induction on the variability in the GM’s risk of infection (rather than the average risk). Variability in risk of infection declined in insects exposed to leaves with increased hydrolyzable tannin levels, and incorporating this information destabilized models of population dynamics and resulted in cyclic behavior (Elderd et al. 2013). An alternative route to enhanced immunity with increasing insect population density is through density-dependent prophylaxis (DPP); that is, animals invest more in parasite resistance when population density is high and the risk of infection is greater (Wilson & Reeson 1998). This would be a response to the cost of immunity preventing the insect from upregulating the immune system on a continual basis. A theoretical analysis of the impacts of DPP on population dynamics (Reynolds et al. 2011) shows that the potential consequences on host population dynamics critically depend on the time delay between the change in density and the increased resistance. As often is the case with theoretical analyses, an array of host dynamics are possible from cyclic to stable depending on conditions. One study on GMs failed to find evidence of DPP (Reilly & Hajek 2008), and Klemola et al. (2007) found no evidence for increased immunity at higher insect densities. The high levels of parasitism at peak host density (Figure 3a) indicate that the immune system is not effectively defending against parasitoids. As WTCs are gregarious from birth until the fifth instar and are thus always exposed locally to high larval densities, it also seems unlikely that this species will demonstrate DPP. This conjecture is supported by an interspecific comparison of solitary and gregarious Lepidoptera that indicated that gregarious species had lower, rather than higher, values for several immune measures (Wilson et al. 2003). Therefore, this hypothesis seems unlikely to be relevant in cyclic population dynamics. Annu. Rev. Ecol. Evol. Syst. 2013.44:565-592. Downloaded from www.annualreviews.org by Lomonosov Moscow State University on 11/28/13. For personal use only. ES44CH26-Myers Changing immunity and conditions that lead to collapse. Changing levels of immunity and a decrease in condition could also trigger the decline at outbreak densities by allowing pathogen prevalence, in particular, to increase, thus leading to further mortality [this is the vicious circles hypothesis by Beldomenico & Begon (2010)]. One trend seen in the dynamics of several forest insects is that fecundity and survival can start to decline before the population peaks (Figure 1b). A possible explanation is that increasingly high population densities result in some level of starvation or detrimental changes in foliage quality, causing reduced immunity and increased susceptibility to pathogens and parasitoids. Experimental data with the AM showed that starvation can alter immunity, but different immune measures changed in opposite directions, making the impact impossible to predict (Yang et al. 2007). The general message is that secondary chemicals have 576 Myers · Cory Annu. Rev. Ecol. Evol. Syst. 2013.44:565-592. Downloaded from www.annualreviews.org by Lomonosov Moscow State University on 11/28/13. For personal use only. ES44CH26-Myers ARI 28 October 2013 15:17 variable effects on different aspects of immunity, which may or may not influence the susceptibility of the insects to parasites. An indication of what might be happening in the field comes from studies on WTCs collected from several sites before, during, and after a population peak, which clearly demonstrated that the condition of the insects declined as density rose (Cory & Myers 2009). Larvae reared from egg masses collected prepeak had very high levels of survival and were disease free, whereas larvae reared in exactly the same manner in the following two years at peak and postpeak densities died from a range of pathogens. Where these pathogens came from is unclear, but given that the rearing conditions were the same each year and the eggs masses were surface-sterilized to remove any contaminating pathogens, as were the leaves used to feed the larvae, it seems most likely that infection resulted from pathogens being carried in a sublethal or latent form by the insects themselves. It is not clear what triggers the expression of these pathogens or how they might be retained within the insects; however, changes in immunity through nutritional stress resulting from high-density insect populations or other as yet unidentified causes are likely mechanisms. Future direction: the role of insect quality in population dynamics. Identifying and explaining changes in insect quality with changes in population density could be an important area for understanding population fluctuations. The interplay between nutrition and susceptibility to disease is part of this. Future direction: plant quality and general disease resistance. Studies should investigate the impact of a broader range of disease-causing microorganisms and use realistic measures of the resistance to disease of field populations in relation to the overall plant quality rather than responses to specific chemicals. Maternal Effects Density-related, delayed intrinsic effects have been suggested as a mechanism for the generation of population cycles in forest Lepidoptera (Rossiter 1994, Inchausti & Ginzburg 2009). Under this scenario, population density in the maternal generation will have an impact on the quality of resulting offspring, mainly through the direct effect of per capita investment or the consequences of altered competition in the offspring environment. This impact will then feed back to population density and result in an interplay between the two. The underlying drivers for these delayed changes in life history characteristics tend to be divided into those related to nutritional factors (primarily leaf quality) and nonnutritional aspects (for example, the impacts of crowding directly), which alter the quality or quantity of egg provisioning (Rossiter 1991). Support for the maternal (or more broadly parental) effects hypothesis for forest insects has been limited (Beckerman et al. 2002). In the analysis of pine looper moth population dynamics by Kendall et al. (2005), densityrelated effects on moth size that in turn influenced offspring performance and density-related parasitism were important in driving the cycles. In general, defoliation resulting from high-density populations clearly influences female pupal weight, and thus fecundity. This is particularly true for capital breeders for which all the resources for reproduction are obtained through feeding as larvae. A majority of outbreak species are capital breeders. Impacts of density and food limitation on offspring quality and vital rates have received little attention. Impact of food quality on survival and offspring quality. Some evidence exists for maternal effects in forest Lepidoptera, but in general, this area has not received much attention. In C. fumiferana, lab studies showed that variation in food quality altered offspring fitness, resulting www.annualreviews.org • Population Cycles in Lepidoptera 577 ARI 28 October 2013 15:17 in poorer offspring survival, but this also resulted in selection for later instars with a greater resistance to starvation and a greater likelihood of surviving diapause (Carisey & Bauce 2002). In GMs collected from field sites with low (<20%) and high (>90%) levels of defoliation, larvae from nutritionally stressed sites had a lower tendency to disperse by ballooning than mothers from less defoliated sites, and they weighed less (Diss et al. 1996). However, no differences were discernible for the longevity of offspring, and impacts on yolk protein were variable. Maternal effects such as development rate and final size of offspring are related to egg size and the order of laying (Wellington 1965, Rossiter 1991), such that larvae from eggs with more yolk do better. In another study on GMs, the number of eggs per mass was related to the density of the field populations and varied from means of 600 to 800 eggs per mass in three low-density populations to means of 200 to 350 eggs per mass for three high-density populations. When reared in the laboratory, the only factor that varied among larvae from eggs from high- and low-density populations was sex ratio; more males developed from high-density populations (Myers et al. 1998). Thus when larvae were reared on artificial media and without the influence of variation in the history of host-plant attack, maternal effects on growth and fecundity were no longer expressed. As with other areas, studies need to focus more on changes in field populations and manipulative experiments that mimic field conditions more closely. Annu. Rev. Ecol. Evol. Syst. 2013.44:565-592. Downloaded from www.annualreviews.org by Lomonosov Moscow State University on 11/28/13. For personal use only. ES44CH26-Myers Delayed immune effects and recovery from declines. Insects that have been exposed to but have survived a pathogen challenge can express various conditions, such as a sublethal effect (cost) from fighting off the pathogen, a persisting covert pathogen infection, or some type of maternal effect (including epigenetic effects) that is passed onto the offspring. In the latter category is transgenerational immune priming, where immunity is up-regulated in the offspring generation (Little et al. 2003). In terms of population dynamics, this is relevant as it could result in delayed protection against pathogens (and other parasites) in one or more generations after population collapse. Immune priming has been demonstrated in several insect species, mainly in response to a variety of bacteria that range in pathogenicity and have been introduced artificially via injection (e.g., Roth et al. 2009, Zanchi et al. 2011). Lepidoptera have been shown to demonstrate immune priming to nonpathogenic bacteria (Freitak et al. 2009). There is also evidence of immune priming to a baculovirus, which reduced susceptibility to the same virus in the offspring generation (Tidbury et al. 2011). An alternative explanation for this result is that the virus persisted as a covert infection. Variation in food quality can also cause immune priming. Larvae reared on poor-quality food showed reduced immunity in the next generation compared with larvae reared on good food (Triggs & Knell 2012). Interestingly this effect was seen through both maternal and paternal routes. The authors suggest two explanations for this: maternal effects or imprinting, such as through some epigenetic mechanism. They suggest that the evidence provides stronger support for the latter. Experiments with the WTC to study the effect of food limitation and virus exposure showed no evidence for changes in resistance to NPV in the offspring with either treatment, despite reductions in moth fecundity and an increase in some measures of immunity in the parental generation (Myers et al. 2011). This result may indicate that some of the measures now routinely used by ecologists to estimate immunity in invertebrates need to be more closely linked to specific pathogen infections for meaningful interpretation (e.g., Saejeng et al. 2010). What is clear from these studies is that many factors can alter immune quality in a transgenerational manner, but the response in terms of the direction of change and the possible interaction among different stressors are harder to predict. Future direction: delayed immune effects. Improved understanding of immunocompetence provides a mechanism that might be relevant to the recovery phase in population cycles if populations become more resistant to virus infection and parasitoids then. Further studies are clearly 578 Myers · Cory ES44CH26-Myers ARI 28 October 2013 15:17 needed on what alters resistance to pathogens and parasitoids across generations, whether there are costs to this resistance, and how this resistance affects insect populations in the field. Annu. Rev. Ecol. Evol. Syst. 2013.44:565-592. Downloaded from www.annualreviews.org by Lomonosov Moscow State University on 11/28/13. For personal use only. Conclusions: Specific Hypotheses Versus General Syndromes Although many fascinating hypotheses have been proposed to explain the population dynamics of forest Lepidoptera, a more synthetic approach is necessary. Parasitism and quality change are consistent characteristics that have been shown to be relevant in the model of the LBM (Turchin et al. 2003) and that of the pine looper moth (Kendall et al. 2005). Models of the GM including viral infection and generalist predators produce cyclic dynamics (Dwyer et al. 2004), although defoliation data show periods of cyclic and noncyclic dynamics (Allstadt et al. 2013). Theoretical models create cyclic dynamics in many ways. The impact of factors that change with population density must be evaluated by a combination of manipulative experiments, quantitative analysis, and mathematical modeling. SYNCHRONY AMONG POPULATIONS AND SPECIES AND WAVES OF SPREAD Another characteristic of forest lepidopteran outbreaks is that they occur over vast distances, and this is most readily apparent from the spatial extent of defoliation that occurs at outbreak densities (Peltonen et al. 2002, Lynch 2012). The widespread patterns of defoliation that sometimes occur give the impression that some cue initiates population increases over large areas simultaneously. Three hypotheses have been proposed for how this synchronicity develops and is maintained. Population fluctuations are synchronized by (a) exogenous weather signals, (b) dispersal among populations, or (c) mobile natural enemies that move among populations. It is very difficult to tease apart the impacts of these three factors, but if weather signals are involved, predictions of how cycles will change with warming environments might be feasible. This would require identifying which of a myriad of weather conditions can strongly influence insect populations. For northern systems this might be severe winter cold killing eggs or conditions that promote the synchrony in bud burst and egg hatch. Spatial Synchrony Synchrony of cyclic dynamics among species and populations has been of interest since the Matamek Conference in 1931 in which the cyclic dynamics of many species and the possible synchronizing factors were discussed (Huntington 1931). An early theoretical consideration of how weather anomalies might synchronize cyclic populations was carried out by Moran (1953), who was working with Dennis Chitty on small mammal cycles (Chitty’s idea and Moran’s model; D. Chitty, personal communication). Moran proposed that two populations with similar dynamics exposed to the same exogenous signal should be synchronized (Bjørnstad et al. 1999). One way to investigate the influence of weather on populations is to examine the spatial relationships between patterns of weather and those of population dynamics (reviewed by Liebhold et al. 2012). The spatial scale of synchrony of populations can be estimated by analyzing correlations among populations at different distances (Bjørnstad et al. 1999). Density changes of populations that are synchronized should be highly correlated. In one example, Peltonen et al. (2002) analyzed landscape-scale, historical outbreak data based on aerial surveys of forest damage for five cyclic forest lepidopteran species: eastern spruce budworms, western spruce budworms (Choristoneura occidentalis), LBMs, FTCs, and introduced GMs. www.annualreviews.org • Population Cycles in Lepidoptera 579 ES44CH26-Myers ARI 28 October 2013 15:17 10,000 Population trend (number of tents) 1,000 Source 100 10 1 0.1 1985 Sink 1990 1995 2000 2005 2010 2015 Annu. Rev. Ecol. Evol. Syst. 2013.44:565-592. Downloaded from www.annualreviews.org by Lomonosov Moscow State University on 11/28/13. For personal use only. Year Figure 5 Trends for two populations of western tent caterpillars on Galiano Island, British Columbia, Canada, one of which is a sink population and the other a source population ( J. H. Myers and J. S. Cory, unpublished data). Although the moth species varied in their dispersal ability from the flightless GM to the more dispersive spruce budworm, the extent and level of synchrony of outbreaks were similar for each species, with population dynamics correlated over a distance of 100–200 km. The decline in the spatial correlation among populations occurred over shorter distances than did those of temperature and precipitation, which were still highly correlated at distances of 700 km. Peltonen and colleagues hypothesized that spatially dependent variation in density-dependent dynamics explained the more rapid decay in population synchrony with distance and this could be associated with variation in factors, such as host-plant quality, that influence populations over shorter distances. Dispersal is probably the least well measured and understood characteristic of cyclic populations of forest caterpillars. Dispersal among populations at the local scale, however, is likely to be common. For example, in the WTC, “sink” populations become extinct locally between outbreaks and thus depend on dispersal from persistent source populations (Figure 5; J. H. Myers and J. S. Cory, unpublished data). This situation can arise if heterogeneity in host-plant species or climatic factors results in some locations being better for positive population growth rates than others (Wellington 1964). In this situation, the increase phases are delayed in the sink population, but the decline phases are synchronous. Even dispersal at relatively short distances, e.g., kilometers, can suffice to synchronize outbreaks. Another example in which spatial synchrony of populations has been evaluated is based on defoliation by GMs in New England (United States), Europe, and Japan ( Johnson et al. 2005). Dominant periodicities of defoliation peaks were significant for only two of the five North American states, whereas four of five European populations had significant dominant periodicities. The patterns of defoliation in New Hampshire and Massachusetts are shown in Figure 6b, and it can be seen that some outbreaks are synchronized between these states, whereas others are not. Particularly early on, populations did not have cyclic dynamics. It is possible that cyclic dynamics started after the establishment of introduced parasitoids (Elkinton & Liebhold 1990), and this might illustrate the influence of parasitoids on the establishment of cyclic population dynamics. These data are further analyzed by Allstadt et al. (2013). Host plants undoubtedly influence the population dynamics of forest Lepidoptera. In a recent analysis of defoliation data for GMs in the northeastern United States from 1975 to 2005, Bjørnstad et al. (2010) found that the periodicity of outbreaks differed between forest types; in dry, oak-pine forests the periodicity of outbreaks was four to five years, whereas in drier, maple-beech-birch 580 Myers · Cory ES44CH26-Myers ARI 28 October 2013 15:17 15,000 Ha defoliated × 1,000 a 10,000 5,000 1934 1944 1954 1964 1974 1984 1994 2004 2014 Year 1,000 Ha defoliated × 1,000 Annu. Rev. Ecol. Evol. Syst. 2013.44:565-592. Downloaded from www.annualreviews.org by Lomonosov Moscow State University on 11/28/13. For personal use only. 0 1924 b New Hampshire Massachusetts 10 0.1 0.001 1924 1934 1944 1954 1964 1974 1984 1994 2004 2014 Year Figure 6 (a) Trends in area defoliated by the gypsy moth in the northeastern United States. Data are plotted on a linear scale to show the decline in the amplitude of the outbreaks in the past ten years. (b) Defoliation data for New Hampshire (red solid circles and line) and Massachusetts (open blue circles and line). These two states are geographically adjacent. Data from the US Forest Service (http://www.na.fs.fed.us/fhp/g/cfm_files/dsp/ dsp_defchart.cfm). forests and intermediate oak-hickory forests the periodicity of outbreaks was nine to ten years with a weak correlation also at four years in the latter (see Figure 6a). This demonstrates the complexity that can occur in cycles of GM defoliation in different forest conditions. Some of the variation in cycles is attributed by Bjørnstad et al. (2010) to small mammal predation on GMs, and Elderd et al. (2013) relate the difference to varying levels of induced defenses between tree species influencing the risk of virus infection of the GM. These hypotheses require experimental testing and comparison to the recent patterns of declining defoliation (Figure 6a). Widespread populations of FTCs in Ontario and Quebec in eastern Canada also vary in their dynamics (Cooke et al. 2011), as indicated by patterns of defoliation. Seven out of nine populations and the region as a whole fluctuated with a periodicity of approximately ten years. One population had infrequent outbreaks. A major outbreak lasting from 1951 to 1954 affected all populations. The densities of populations less than 100 km apart were highly correlated. These populations illustrate how regional dynamics can be quite variable, but also synchronized at some times such as was observed in 1951–1954. www.annualreviews.org • Population Cycles in Lepidoptera 581 ARI 28 October 2013 15:17 In Fennoscandia, Klemola et al. (2006) identified clusters of populations with synchronous dynamics and positive cross correlations in population growth rates. The strongest synchrony was within regional clusters, where moths shared similar environments. Synchrony was observed over distances of 700 km, which is further than that for other species mentioned above. Southern populations still cycled but with less amplitude. Synchrony between species or genetically distinct biotypes more likely reflects exogenous inputs such as weather anomalies or the impacts of common parasitoids. One such situation involves LBM populations in France and Switzerland (Dormont et al. 2006). Two genetically distinct biotypes of LBM exist, one that feeds on subalpine larch and the other on Cembran pine. In both areas where populations have been monitored, peak densities have been within a year of each other. Little is known about whether these two biotypes share parasitoids but it is likely that they do. As discussed above, another European example of population synchrony between genetically distinct species involves AMs and WMs that attack the same birch trees in Fennoscandia (Tenow et al. 2007). These reach peak densities one or two years out of phase. Therefore, although they experience the same climate and have the same food plants, some factor is influencing their dynamics in slightly different ways. Mutual parasitoids could again be a factor, and different levels of predation could influence the two species differentially. After the population decline, parasitism of experimentally released AM larvae was high, which indicates that parasitoids remained common after the decline of the AM and with continued high density of the WM (N. Klemola et al. 2008). In conclusion, in most cases synchrony of insect population dynamics drops off at shorter scales than does the spatial similarity in temperature and precipitation. A difficulty with these studies is identifying what type of weather anomaly might be relevant to insect populations (see below). Annu. Rev. Ecol. Evol. Syst. 2013.44:565-592. Downloaded from www.annualreviews.org by Lomonosov Moscow State University on 11/28/13. For personal use only. ES44CH26-Myers Waves of Outbreak Spread In contrast to the widespread synchrony of population outbreaks is the occurrence of spatial waves of outbreaking populations over geographical space. Based on 40 years of monitoring of defoliation caused by the LBM, directional waves of spread were identified that travel from the western edge of the larch forest distribution across the European Alps at a rate of 220 km/year. Models based on host-parasitoid interactions support this observation as long as dispersal is directionally biased or habitat quality varies across the landscape (Bjørnstad et al. 2002). In Fennoscandia, waves of AM and WM outbreaks were observed to spread over an approximately 10-year period beginning in the northeast in eastern Finland and the border with Russia in 1991, and moving westward and southward to reach the islands off the coast of Norway in 2000 (Tenow et al. 2007). The most recent analysis of the geographical structure of outbreaks of WMs and other geometrids is based on six decades of data (Tenow et al. 2012; Figure 7). In each decade a wave of outbreaks moved across Europe from ESE-WNW toward the Scandes and the Atlantic Ocean, approximately a 3,000-km distance, at an average speed of 330 km/year. Tenow et al. (2012) propose that stand isolation beyond the forest steppe zone to the east creates a hostile zone for WMs, whereas in suitable habitats to the west, within-patch outbreaks are synchronized by short-distance dispersal and perhaps more mobile and density-delayed parasitoids. The geographical dynamics of the spread of moths in the family Geometridae, including AMs and WMs, was further elucidated using satellite data in the next period of outbreaks from 2000 to 2008 ( Jepsen et al. 2009). This new technology allowed monitoring of both defoliation and temperature patterns that relate to leaf phenology. The patterns of moth spread varied across the cycle. In the incipient phase, defoliation started at many locations and was highly synchronous. This resulted in long spread distances of 20–80 km being common. In the epidemic and crash phases, spread distances were much shorter (0–15 km). The satellite data also indicated large-scale 582 Myers · Cory ES44CH26-Myers ARI 28 October 2013 15:17 2010 2005 2000 1995 Year of outbreak 1990 1985 1980 1975 1970 Annu. Rev. Ecol. Evol. Syst. 2013.44:565-592. Downloaded from www.annualreviews.org by Lomonosov Moscow State University on 11/28/13. For personal use only. 1965 1960 1955 1950 1945 –1,000 –500 0 500 1,000 1,500 2,000 2,500 3,000 Distance from western baseline (km) Figure 7 Regressions of the relationships of outbreak occurrences to year for the decadal spread of winter moth and associated geometrids in northern Europe. Each colored line indicates the geographic spread of population outbreaks across Finland, Sweden, and Norway from approximately the border with Russia and going west to the Atlantic Ocean. Regression lines are based on data from Tenow et al. (2012). The x-axis is the distance from the western baseline that is parallel to the Norwegian coast and the y-axis is the year of outbreak. Each wave lasts approximately 10 years and covers a distance of approximately 3,000 km. Slopes of the lines vary slightly, indicating differences in the speeds of the waves, and line lengths are influenced by the available data on outbreaks. synchronization of spring phenology of plant growth during the incipient phase of the cycle. Jepsen et al. (2009) conclude that these patterns support a synchronizing Moran effect acting through phenological synchronization of egg hatch and bud development at the early stages of outbreak, followed by dispersal (diffusion) as the outbreak progresses. A problem with satellite data is that defoliation caused by AMs is indistinguishable from that caused by WMs, and the occurrence of waves was not recognized in this study (O. Tenow, personal communication). Therefore, although satellite data can be useful for looking at broad patterns of insect outbreaks, it is important to also include the details of the system. Future direction: use of satellite data to study spatial synchrony in outbreaks. Tenow et al. (2012) conclude that knowledge of wave patterns is necessary for understanding local outbreaks and that isolated local or even regional studies alone cannot explain the large-scale, spatio-temporal dynamics of outbreaks of WMs. Satellite data are now available for looking at widespread patterns relevant to the phenological synchrony of insects and their food plants, and these should be applied to other systems. But they also require careful ground-truthing. Future direction: roles of dispersal of moths and parasitoids in synchronizing populations. More information on the movement of parasitoids, the dispersal of moths, and the identification of unique weather conditions that could periodically synchronize populations is required. Looking at the similarity of correlations between defoliation and weather is not sufficient to identify causation. www.annualreviews.org • Population Cycles in Lepidoptera 583 ES44CH26-Myers ARI 28 October 2013 15:17 Climate Change and Outbreaks of Forest Lepidoptera Annu. Rev. Ecol. Evol. Syst. 2013.44:565-592. Downloaded from www.annualreviews.org by Lomonosov Moscow State University on 11/28/13. For personal use only. Population cycles of forest Lepidoptera tend to be more apparent in northern areas and at higher elevations. Thus it might be predicted that warming climates will disrupt population dynamics to a greater extent in these areas. Already, tree ring data from forests inhabited by the LBM show that warming climates could influence the distribution of insects and their host trees and thus change the location of the epicenters of population outbreaks ( Johnson et al. 2010). Based on tree ring data, Büntgen et al. (2009) demonstrate consistent cycles of the LBM between 1700 and 2000. They report that though the periodicity of local outbreaks continues, alpinewide defoliation no longer occurs in Switzerland. Further analysis using isotopic signatures of tree rings showed that below average July to August temperatures were coupled with defoliation events over more than three centuries (Kress et al. 2009). Although the amplitude of LBM population cycles in the French Alps has declined two-and-a-half to six times since 1985, population peaks have continued to occur with the typical 8–9 year periodicity (A. Roques, personal communication). Although not likely to be the only factor related to population outbreaks, climate, including both temperature and rain, has the potential to influence population growth rates, food availability, disease susceptibility, and the phenological relationships between insects, their food plants, and their natural enemies (Both et al. 2009; reviewed by Lynch 2012). Patterns are unlikely to be simple, and the literature on the relationship of temperature to cycles of forest Lepidoptera is contradictory. Cool temperatures and precipitation are positively associated with population outbreaks in several studies. For example, tree ring analysis shows that outbreaks of C. occidentalis do not occur in years of drought, whereas C. fumiferana tends to outbreak in dry springs (Lynch 2012). A breakdown in cycles of the LBM was attributed to warm springs followed by cool summers (Baltensweiler 1993), whereas Kress et al. (2009) found that defoliation by the LBM was associated with cool summers. This is impossible to interpret. Myers (1998) suggested that the high number of population outbreaks that occurred over the mid-1950s (40% of 26 species had outbreaks in 1956 and 25% in 1954) might have been associated with cool temperatures. If this were true, warmer climates could reduce the frequency of outbreaks. For WTC populations, temperature and rate of population growth have been negatively related over the time period of 2000 to 2012 (r2 = 0.52; J. H. Myers and J. S. Cory, unpublished data) though the amplitudes of outbreaks have not changed over the past four cycles. Future direction: the role of cool summers. Cool temperatures have been associated with population outbreaks in several studies. Mechanisms that might lead to this association should be identified and more detailed relationships between population growth and temperature should be measured. Future direction: continued cycles at lower population density. A most intriguing characteristic that needs to be explained is the continued periodicity of cycles in species such as the LBM and the AM for which amplitudes of outbreaks have declined (Figure 3a for the AM). How density-related factors thought to drive population cycles function when populations do not reach outbreak densities but continue to cycle is a fascinating mystery. Climate Warming and Phenological Mismatch One of the key impacts of climate warming on populations could be phenological mismatch (Miller-Rushing et al. 2010). The hypothesis that changing climate could influence insect 584 Myers · Cory Annu. Rev. Ecol. Evol. Syst. 2013.44:565-592. Downloaded from www.annualreviews.org by Lomonosov Moscow State University on 11/28/13. For personal use only. ES44CH26-Myers ARI 28 October 2013 15:17 populations through modification of the timing of egg hatch to bud burst is most apparent in studies of WMs (van Asch & Visser 2007). As mentioned above, widespread synchronization of the onset of the growing season and leafing of birch was apparently related to outbreaks of AMs and WMs ( Jepsen et al. 2009). This could have acted through synchronization of egg hatch and budburst. In several cases the impact of mismatch between egg hatch and bud burst has been tested experimentally. Baltensweiler (1993) modified the hatch of LBM eggs through shading. Delayed hatch in a warm spring synchronized the larvae beneficially with bud burst, whereas early hatch was detrimental. For GMs, delayed egg hatch was advantageous overall because even though food quality was poor for late-hatching larvae, this reduced their density and they experienced lower attack from a parasitoid that responded to host density (Hunter & Elkinton 2000). Delayed egg hatch had no apparent influence on larval development of the WTC (Myers 1992). In a unique branch-level warming experiment with the WTC (H. Kharouba, M. Vellend, R. M. Sarfraz, and J. H. Myers, submitted), larvae that hatched two to three weeks before bud burst did not have reduced larval growth, development, or survival. This agrees with Singer & Parmesan (2010), who point out that species might not have evolved close phenological synchrony with bud burst but rather maintain flexibility to respond to temporal variability in weather conditions. Thus, they maintain the potential to adapt to changing environments. The level of adaptation is likely to vary among species and environments. Future direction: temperature influences on plant and insect phenology. Determining how temperature influences the relationships between bud burst and egg hatch and how this affects the survival rates of life-history stages will be critical to the prediction of responses of populations to climate change. Some species may be much more resilient to mismatch than others and this could relate to whether they develop to larvae in the eggs before or after diapause. Future direction: heterogeneity in phenological relationships across species ranges. Variability in weather patterns across a species’ range might influence selection on budburst and egg hatch phenology. Further experimental work should be done to determine whether generalizations can be made about the importance of phenological mismatch to cyclic dynamics among sites and species. CONCLUSIONS In Table 1 we summarize information on seven species of cyclic forest Lepidoptera and list some questions that arise for future work. Even with all of the work that has gone on in the past 25 years on cycling forest Lepidoptera, it is still a mystery as to how such a regular pattern of population dynamics can be maintained for so long, how consistent waves of spread can persist for some species but not others, and how populations can continue to cycle at low densities in phase with outbreak populations. The biggest black box that remains is the extent of dispersal among populations, and the relation of this to traveling waves should be a major focus in the future. Just how warming climates will change population dynamics and distributions is still uncertain, and it is important to differentiate between projections and observations in this regard. Some clear generalities exist as cyclic species are similar in their population trends, relationships with parasitoids, and changes in fecundity over the cycle. www.annualreviews.org • Population Cycles in Lepidoptera 585 586 Northern Europe: Fennoscandia. Outbreaks do not occur in southern Finland Europe: Fennoscandia and Holarctic European Alps Autumnal moth (AM) Winter moth Larch budmoth Range Myers · Cycle Cory 9–10 years 9–10 years 9–10 years length Declining amplitude of peaks Continuing traveling waves of outbreaks Decreasing peak densities with poor recovery of mountain birch after defoliation Current status Traveling waves Traveling waves Traveling waves trends Population Relevant factors Changes in food quality and parasitism associated with declines Often lag behind outbreaks in AM Outbreaks less high at coast High pupal predation High parasitism and decreasing size at peak Defoliation in some areas at higher elevations and lower densities at coastal sites Unanswered questions (Continued ) What is the influence of warm summers on population success as current suggestions are conflicting? Are population epicenters changing with warming climates? How does dispersal relate to traveling waves? What allows continued high density following AM outbreaks? Does infection by CPV or NPV play a role at peak density? What factors cause continued cycles in areas without defoliation? How much and what is the form of dispersal required to synchronize populations and cause traveling waves? Does infection by a cypovirus (CPV) or nucleopolyhedrovirus (NPV) play a role at peak density? What factors cause continued cycles in areas without defoliation? 28 October 2013 Subalpine larch and Cembran pine Birch and oak Primarily mountain birch Host plants ARI Species Table 1 Summary of characteristics of seven cyclic species of forest Lepidoptera, factors thought to be relevant to their cyclic dynamics, and unanswered questions for future research Annu. Rev. Ecol. Evol. Syst. 2013.44:565-592. Downloaded from www.annualreviews.org by Lomonosov Moscow State University on 11/28/13. For personal use only. ES44CH26-Myers 15:17 Northeastern North America Eastern spruce budworm Spruce-fir forests Primarily trembling aspen trees, pure and mixed stands Red alder, apple, cherry, rose, currant 30–40 years ∼10 years, varies 6–11 years Harmonic oscillations of 4–5 and 8–10 years with periods of noncyclic dynamics No apparent change Cyclic dynamics unchanged Cyclic dynamics unchanged Decreasing peak amplitudes with subharmonics in defoliation data Greater defoliation in eastern areas with decline to west (New Brunswick to western Ontario) Geographical variation in synchrony in Ontario and Quebec; duration of peak related to fragmentation Island populations remain synchronous Spreading distribution Deteriorating forest condition, reduced survival of early instar larvae, and delayed impact of natural enemies cause decline and slow recovery Parasitism and viral infection cause decline and generalist predators have a role at low densities Reduced fecundity, viral infection, and parasitism change with density Parasitoids, fungus, and control procedures reduce population levels Density-related infection causes declines Will warming climates influence areas of defoliation? Does variation in predation influence the rate of increase of FTC between mixed and pure forest stands of aspen? What is the role of dispersal in maintaining synchrony? What reduces fecundity over late increase and into population decline? How is virus maintained at low host density? What is the role of viral infection in populations with low amplitude peaks and at the front of the spread in distribution? What is the relation of defoliation to moth population dynamics? Why is the amplitude of peaks of defoliation and duration of outbreak declining? 28 October 2013 Primarily across northern North America Primarily coastal North America Western tent caterpillar Primarily oaks but highly polyphagous ARI Forest tent caterpillar (FTC) Introduced to North America Gypsy moth Table 1 (Continued ) Annu. Rev. Ecol. Evol. Syst. 2013.44:565-592. Downloaded from www.annualreviews.org by Lomonosov Moscow State University on 11/28/13. For personal use only. ES44CH26-Myers 15:17 www.annualreviews.org • Population Cycles in Lepidoptera 587 ES44CH26-Myers ARI 28 October 2013 15:17 DISCLOSURE STATEMENT The authors are not aware of any affiliations, memberships, funding, or financial holdings that might be perceived as affecting the objectivity of this review. ACKNOWLEDGMENTS Annu. Rev. Ecol. Evol. Syst. 2013.44:565-592. Downloaded from www.annualreviews.org by Lomonosov Moscow State University on 11/28/13. For personal use only. We dedicate this review to the memory of Werner Baltensweiler. We acknowledge the incredible work that has been done over the years by Olle Tenow, Erkki Haukioja, and Tero Klemola and colleagues that has contributed so much to our understanding of population cycles. We thank Tero Klemola, Charles Krebs, Olle Tenow, Greg Dwyer, Bruce Kendall, Laurent Dormont, Alain Roques, Jens Roland, and Helena Bylund for providing data, helpful comments on the manuscript, and/or answering our questions. Isla Myers-Smith has taken after her father in her ability to wield the red pen and helped greatly. Charles Krebs and Dennis Chitty were mentors to J.H.M. and have provided many useful discussions over the years. Finally we greatly appreciate the students who have contributed to our work on tent caterpillars. Together we have reared more caterpillars than we like to remember. NSERC Canada provided funding for our own work that is presented here. LITERATURE CITED Allstadt AJ. 2013. Long-term shifts in the cyclicity of outbreaks of a forest-defoliating insect. Oecologia 172:141– 51 Baltensweiler W. 1993. Why the larch bud moth cycle collapsed in the subalpine larch-cembran pine forests in the year 1990 for the first time since 1850. Oecologia 94:62–66 Baltensweiler W, Benz G, Bovey P, Delucchi V. 1977. Dynamics of larch bud moth populations. Annu. Rev. Entomol. 22:79–100 Baltensweiler W, Fischlin A. 1988. The larch budmoth in the Alps. 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Downloaded from www.annualreviews.org by Lomonosov Moscow State University on 11/28/13. For personal use only. ES44CH26-Myers 592 Myers · Cory ES44-FrontMatter ARI 29 October 2013 12:6 Contents Annual Review of Ecology, Evolution, and Systematics Volume 44, 2013 Annu. Rev. Ecol. Evol. Syst. 2013.44:565-592. Downloaded from www.annualreviews.org by Lomonosov Moscow State University on 11/28/13. For personal use only. Genomics in Ecology, Evolution, and Systematics Theme Introduction to Theme “Genomics in Ecology, Evolution, and Systematics” H. Bradley Shaffer and Michael D. Purugganan p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1 Genotype-by-Environment Interaction and Plasticity: Exploring Genomic Responses of Plants to the Abiotic Environment David L. Des Marais, Kyle M. Hernandez, and Thomas E. Juenger p p p p p p p p p p p p p p p p p p p p p p 5 Patterns of Selection in Plant Genomes Josh Hough, Robert J. Williamson, and Stephen I. Wright p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p31 Genomics and the Evolution of Phenotypic Traits Gregory A. Wray p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p51 Geographic Mode of Speciation and Genomic Divergence Jeffrey L. Feder, Samuel M. Flaxman, Scott P. Egan, Aaron A. Comeault, and Patrik Nosil p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p73 High-Throughput Genomic Data in Systematics and Phylogenetics Emily Moriarty Lemmon and Alan R. Lemmon p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p99 Population Genomics of Human Adaptation Joseph Lachance and Sarah A. Tishkoff p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 123 Topical Reviews Symbiogenesis: Mechanisms, Evolutionary Consequences, and Systematic Implications Thomas Cavalier-Smith p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 145 Cognitive Ecology of Food Hoarding: The Evolution of Spatial Memory and the Hippocampus Vladimir V. Pravosudov and Timothy C. Roth II p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 173 Genetic Draft, Selective Interference, and Population Genetics of Rapid Adaptation Richard A. Neher p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 195 Nothing in Genetics Makes Sense Except in Light of Genomic Conflict William R. Rice p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 217 v ES44-FrontMatter ARI 29 October 2013 12:6 The Evolutionary Genomics of Birds Hans Ellegren p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 239 Community and Ecosystem Responses to Elevational Gradients: Processes, Mechanisms, and Insights for Global Change Maja K. Sundqvist, Nathan J. Sanders, and David A. Wardle p p p p p p p p p p p p p p p p p p p p p p p p p 261 Cytonuclear Genomic Interactions and Hybrid Breakdown Ronald S. Burton, Ricardo J. Pereira, and Felipe S. Barreto p p p p p p p p p p p p p p p p p p p p p p p p p p p p 281 Annu. Rev. Ecol. Evol. Syst. 2013.44:565-592. Downloaded from www.annualreviews.org by Lomonosov Moscow State University on 11/28/13. For personal use only. How Was the Australian Flora Assembled Over the Last 65 Million Years? A Molecular Phylogenetic Perspective Michael D. Crisp and Lyn G. Cook p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 303 Introgression of Crop Alleles into Wild or Weedy Populations Norman C. Ellstrand, Patrick Meirmans, Jun Rong, Detlef Bartsch, Atiyo Ghosh, Tom J. de Jong, Patsy Haccou, Bao-Rong Lu, Allison A. Snow, C. Neal Stewart Jr., Jared L. Strasburg, Peter H. van Tienderen, Klaas Vrieling, and Danny Hooftman p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 325 Plant Facilitation and Phylogenetics Alfonso Valiente-Banuet and Miguel Verdú p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 347 Assisted Gene Flow to Facilitate Local Adaptation to Climate Change Sally N. Aitken and Michael C. Whitlock p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 367 Ecological and Evolutionary Misadventures of Spartina Donald R. Strong and Debra R. Ayres p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 389 Evolutionary Processes of Diversification in a Model Island Archipelago Rafe M. Brown, Cameron D. Siler, Carl H. Oliveros, Jacob A. Esselstyn, Arvin C. Diesmos, Peter A. Hosner, Charles W. Linkem, Anthony J. Barley, Jamie R. Oaks, Marites B. Sanguila, Luke J. Welton, David C. Blackburn, Robert G. Moyle, A. Townsend Peterson, and Angel C. Alcala p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 411 Perceptual Biases and Mate Choice Michael J. Ryan and Molly E. Cummings p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 437 Thermal Ecology, Environments, Communities, and Global Change: Energy Intake and Expenditure in Endotherms Noga Kronfeld-Schor and Tamar Dayan p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 461 Diversity-Dependence, Ecological Speciation, and the Role of Competition in Macroevolution Daniel L. Rabosky p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 481 Consumer Fronts, Global Change, and Runaway Collapse in Ecosystems Brian R. Silliman, Michael W. McCoy, Christine Angelini, Robert D. Holt, John N. Griffin, and Johan van de Koppel p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 503 vi Contents ES44-FrontMatter ARI 29 October 2013 12:6 Implications of Time-Averaged Death Assemblages for Ecology and Conservation Biology Susan M. Kidwell and Adam Tomasovych p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 539 Population Cycles in Forest Lepidoptera Revisited Judith H. Myers and Jenny S. Cory p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 565 Annu. Rev. Ecol. Evol. Syst. 2013.44:565-592. Downloaded from www.annualreviews.org by Lomonosov Moscow State University on 11/28/13. For personal use only. The Structure, Distribution, and Biomass of the World’s Forests Yude Pan, Richard A. Birdsey, Oliver L. Phillips, and Robert B. Jackson p p p p p p p p p p p p p p p 593 The Epidemiology and Evolution of Symbionts with Mixed-Mode Transmission Dieter Ebert p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 623 Indexes Cumulative Index of Contributing Authors, Volumes 40–44 p p p p p p p p p p p p p p p p p p p p p p p p p p p 645 Cumulative Index of Article Titles, Volumes 40–44 p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 649 Errata An online log of corrections to Annual Review of Ecology, Evolution, and Systematics articles may be found at http://ecolsys.annualreviews.org/errata.shtml Contents vii