The Elements of Seasonal Adaptations in Insects

1 The elements of seasonal adaptations in insects

H.V. Danks Biological Survey of Canada (Terrestrial Arthropods), Canadian Museum of Nature, P.O. Box 3443, Station D, Ottawa, Ontario, Canada K1P 6P4 (e-mail: [email protected])

Abstract—The many components of seasonal adaptations in insects are reviewed, especially from the viewpoint of aspects that must be studied in order to understand the structure and purposes of the adaptations. Component responses include dispersal, habitat selection, habitat modification, resistance to cold, dryness, and food limitation, trade-offs, diapause, modifications of developmental rate, sensitivity to environmental signals, life-cycle patterns including multiple alternatives in one species, and types of variation in phenology and development. Spatial, temporal, and resource elements of the environment are also reviewed, as are environmental signals, supporting the conclusion that further understanding of all of these seasonal responses requires detailed simultaneous study of the natural environments that drive the patterns of response.

Résumé—On trouvera ici une revue des multiples composantes des adaptations saisonnières des insectes, particulièrement des aspects à examiner afin de comprendre la structure et les buts de ces adaptations. Ces composantes incluent la dispersion, la sélection d’habitat, la modification d’habitat, la résistance au froid, à la sécheresse et aux restrictions de nourriture, les compromis, la diapause, les modifications du taux de développement, la sensibilité aux signaux environnementaux, les patrons de cycles biologiques (y compris les patrons multiples possibles chez une même espèce), ainsi que les types de variation dans la phénologie et le développement. La revue considère aussi les conditions d’espace, de temps et de ressources dans le milieu de même que les signaux environnementaux. En conclusion, la compréhension accrue de ces réponses saison- nières requiert une étude détaillée et simultanée des environnements naturels qui régissent les patrons de réponses.

[Traduit par la Rédaction]

Danks44 Table of contents Developmental modifications 22 Sensitivity to environmental signals 23 Introduction 1 Life-cycle patterns 25 Elements of the habitat 2 Types of variation 26 Spatial framework 2 Conclusions 29 Temporal framework 3 References 30 Resources and limitations 4 Signals 5 Introduction Elements of the response 6 Spatial framework 6 The extensive literature about insect season- Temporal framework 7 ality reveals great diversity and complexity in Resources and limitations 9 the adaptations that withstand seasonal adver- Modification of adverse conditions 9 sity and synchronize development with the sea- Resistance to adversity 10 sons. This paper reviews the basic structure of Cold 10 these adaptations, identifying the elements that Dryness 13 are needed to characterize a given life cycle and Food limitation 16 hence serving too to identify the decisions Trade-offs 17 needed in planning investigations. Treating this Responses in extreme habitats 19 broad subject area in detail would require sev- Control and integration 22 eral books, but the aim here is to provide a

Received 25 May 2006. Accepted 12 September 2006.

Can. Entomol. 139: 1–44 (2007) © 2007 Entomological Society of Canada 2 Can. Entomol. Vol. 139, 2007 shorter treatment that gives the necessary over- on regional patterns of climate. Such large-scale view and essential details in one place, in the patterns may also have been modified by the his- hope that such a treatment will be of value to a torical processes of glaciation, isolation, and ge- range of readers. The approach therefore is syn- netic drift (e.g., Armbruster et al. 1998; Bossart optic rather than comprehensive, but relevant 1998; Stone et al. 2001). literature, especially reviews and recent papers, Intermediate spatial complexity, such as com- is cited to lead into the wider literature on each plex topography, influences dispersal and thus topic. Specific practical aspects have been interpopulation variation in species with limited treated by Danks (1987a, chap. 14, 1996, capacity for movement (Wishart and Hughes 2000c). 2001). Certainly, there is much evidence for Most accounts of insect seasonality focus im- heritable variation in life-history traits for popu- mediately on the organisms’ responses, such as lations from different habitats, for example be- photoperiodism. I begin instead with the impor- tween closed woodlands and open landscapes tant environmental context, because unravelling that are warmer (Karlsson and Van Dyck 2005) or the responses requires an understanding of the between habitats at different elevations (Sorensen characteristics and complexity of natural envi- et al. 2005). In particular, because local selection ronments. Spatial, temporal, and resource- favours specific life-cycle adaptation but inter- limited elements of the responses are then out- breeding offsets regional differentiation, knowing lined, including the ways in which insects deal about dispersal, range size, and other factors with seasonal adversity, followed by an account that interact with local habitat features such as of the ways in which the responses are con- growing season and resource distribution helps trolled and integrated. scientists to interpret seasonal adaptations and voltinism (cf. Dennis et al. 2000; Llewellyn et Elements of the habitat al. 2003). Habitat suitability at the local level comprises Habitats vary in space and time on a variety many elements beyond the general effects of of different scales. Small-scale spatial influ- climatic differences. For example, complex in- ences, notably the role of microhabitats, are teractions with host-plant phenology are known. especially important for insects, but they oper- Host plants may or may not coincide with the ate in the context of much larger patterns (for seasons in the same way as their herbivores, example, compare Corbet 1972; Oke 1987; creating differences in suitability from one Bailey et al. 1997). Adaptations are a result of place to the next. The fitness of many herbi- changes not just on seasonal time frames but vores depends on the close synchrony of egg also over longer and shorter intervals, and re- hatch with bud burst (e.g., Chen et al. 2003) or flect too the evenness or predictability of the on the quality of leaves at particular times of changes. year. Leaf quality tends to decline rapidly after Habitats provide both resources (such as spring, and again towards the end of the season. food) and constraints (such as cold winters). Summer leaves vary less, increasing the range Depending on time and place, therefore, insects of developmental durations that are possible in require a resistant stage during adversity and an species that feed during the middle of the sea- active stage during conditions that can be ex- son (cf.Foxet al. 1997; Kause et al. 2001). ploited for development or reproduction. Habi- Smaller scale influences are also known. For tats also differ in how visibly or reliably they example, modelling for one butterfly population provide signals from which current or future showed that locating larvae differently within conditions can be assessed. Consequently, the the habitat can change phenology by up to analysis of insect habitats in the context of life 11 days (Weiss and Weiss 1998). Differences cycles must address a range of elements: spatial among microhabitats are also critical to winter and temporal frameworks, resources and limita- survival. Thus, depending on locality and year, tions, and signal features. survival of the boll weevil Anthonomus grandis Boheman (Curculionidae) overwintering in lit- Spatial framework ter varies from 0% to 100% (Pfrimmer and The spatial complexity of habitats is one tem- Merkl 1981). Differences in survival can de- plate for the evolution of seasonal adaptations. pend on many very small-scale features, such as At the largest scale, the presence and intensity of local vegetation (which holds up snow) and developmental delays such as diapause depend whether it dies back seasonally, and surface

© 2007 Entomological Society of Canada Danks 3 depressions (which accumulate water or snow especially dangerous to synchronized cohorts. and may reduce the impact of fires) (Danks Again, their effect depends on the mean tem- 1991b). perature (cf. Table 1). Variability from year to year makes suitable Temporal framework habitats or resources different in amount or in Habitat suitability, driven chiefly by climatic timing from one year to the next, threatening suitability, depends on how far conditions de- species without ways to modify fixed modes of part from those allowing development and on development. The effects of long-term extremes their seasonal pattern, but it depends also on the that differ greatly from the mean depend on the extent of variation both within and among years mean temperature. For example, subfreezing (Danks 1999). Differences in these parameters temperatures can occur in arctic summers (as are exemplified by data for a small number of noted above for the shorter term) and unusual sample sites shown in Table 1. Of course, many heat in subtropical summers (Table 1). The con- more climate types and gradations have been sequences of inter-seasonal variability have sel- recognized, including a range of alpine, desert, dom been quantified but may be more pervasive tropical, and oceanic climates (e.g., Hodkinson than is usually considered. For example, 2005a; Oliver 2005; Turnock and Fields 2005). Östman (2005) concluded that large-scale year- However, the sample locations in Table 1 serve to-year variations are more important to the sur- to illustrate key habitat characteristics for in- vival and fecundity of carabid populations than sects. are spatial variations over the shorter term. Severity reflects temperatures that are too cold Likewise, the role of long-term climatic pat- or too hot, heat sums inadequate for develop- terns (as opposed to more random variations), ment, and moisture regimes that are too dry. For such as those driven by the El Ninõ or North example, winter temperatures range, chiefly ac- Atlantic Oscillation effects (cf. Dettinger and cording to latitude, from extremely cold to Diaz 2000), has been assessed only in a limited warm, while summer temperatures range from way but can significantly alter insect phenology cool to hot (Table 1). The effect of temporal and other traits (Briers et al. 2004). variation in conditions depends on the average Climatic factors, especially the driving vari- condition. For example, in the high Arctic, ables of temperature and precipitation, affect where mean maximum temperatures in summer different habitats in different ways. Protected are only a few degrees above 0 °C, day-to-day habitats change more slowly and have a nar- variation makes summer frosts very likely (cf. rower range of extremes than exposed ones Table 1). This likelihood is up to 90% even in (cf. Danks 1971a). Typical tropical streams the warmest month (Danks 1993, Table 1). In have relatively steady flow, whereas at high lat- turn, severe climates influence the occurrence itudes seasonal differences in precipitation and of host plants and other foods. Coping with se- evapotranspiration usually are more marked and verity requires resistance such as cold hardi- contributions from winter snow and ice are de- ness, selection of microhabitats that are layed (Dettinger and Diaz 2000). In desert re- buffered against the extremes of heat, cold, or gions, rainfall is especially variable from year dryness, daily and annual timing of activity, and to year, and stream flow is more variable still so on. (Dettinger and Diaz 2000). Moreover, stream Timing and other adaptations are likewise re- flow varies on still smaller scales (Lytle 2002; quired to allow for seasonality, conditions that Benbow et al. 2003). change across an annual time frame so that typ- Key characteristics of conditions at the level ically they are suitable for development and of habitat are therefore difficult to quantify be- reproduction only part of the time. Seasonal cause of their variability and unpredictability. conditions are commonly assessed by seasonal For example, the “dryness” of deserts depends differences and variations in temperature on the variability and predictability of rainfall (cf. Table 1), but many other environmental fac- as well as on its absolute amount (Noy-Meir tors influence suitability (see Resources and 1973). Some variables affect life cycles in some limitations). years but not in others (e.g., Fleishman et al. Unpredictable short-term patterns include 1997). Similar intermittent influences are ex- variation within a given month. Marked erted by rare catastrophic events such as fires, changes of this sort, for example sudden spells flooding, and drought. For example, depending of hot or cold, drought or flooding, may be on the terrain and the stand type, the mean time

Table 1. Sample measures of severity, seasonality, unpredictability, and variability in zones with different

Severity

Annual heat W mean W mean air C mean air accumulation,* day- precip., Zone temp., °C temp.,°C deg. above 0 °C mm 1. High Arctic 4.6 –33.7† 250 21 2. Low Arctic 7.9 –26.5 633 53 3. North temperate central continental 19.3 –17.6 2210 60 4. North temperate eastern continental 20.7 –10.8 3067 78 5. North temperate maritime 15.4 –4.3 2128 89 6. South temperate continental 26.7 7.5 6237 131 7. Seasonal tropical 29.4‡ 26.1§ 9974 76 8. Wet tropical 25.8† 24.3 9261 261 9. Desert 20.9¶ 15.4** 6470 0.1 Note: W, warmest month (typically July); C, coldest month (typically January). Summer is the warmest 6 months Canada (52°N); 4, Ottawa, ON, Canada (45°N); 5, St. John’s, NL, Canada (45°N); 6, Birmingham, AL, United States of and Orvig (1970); Court (1974); Hare and Hay (1974); Miller (1976); Portig (1976); and Ratisbona (1976). *Heat accumulations are indicative only, based on monthly mean screen-air temperatures. †February. ‡May. §December. ||February–August (93% May–October). ¶January. **July. ††October–May. between fires in many boreal coniferous forests threshold to complete the life cycle, but there is only about 50 to 100 years, a shorter period are very wide variations among species (Hon.k than the intrinsic generation time of the trees and Kocourek 1990; Danks 2006c). The impact (Danks and Foottit 1989). Variations in differ- of temperature is modified by habitat, and most ent habitats over intervals of more than one other physical conditions and resources are in- year include marked changes in salinity (e.g., tegrated with other factors. For example, oxy- Garcia et al. 1997), nutrient level, and other gen levels depend on flow rate and microhabitat features. How organisms cope with such inter- (e.g., Genkai-Kato et al. 2005). Even in simple mittent challenges is therefore relevant to their situations, food availability integrates the sea- success. They must not only follow annual cy- sonal supply of heat, light, water, and so on. cles that accord with seasonality and withstand Most biotic influences are complex because or- long periods each year with very low tempera- ganisms interact with one another: the effects of tures or limited rainfall, but also survive unpre- parasites, predators, diseases, and competitors dictable events. on seasonal suitability are dynamic as populations develop and interact. In some species bi- Resources and limitations otic rather than physical factors cause most Among physical elements, temperature is the winter mortality, even where temperatures are most critical habitat factor, tied closely to cli- low (cf. Pitts and Wall 2005). mates (see above) and effective through lower Therefore, depending on the time of year, and upper limits and through heat accumula- most habitats have positive elements when they tion. Lower developmental limits for insects av- provide resources and favour development and erage about 10 or 11 °C (Utida 1957; Hon.k negative elements when physical conditions are and Kocourek 1990) and in most temperate spe- untenable and resources are inadequate. As- cies upper limits lie between 20 and 35 °C (un- sessing the setting of individual species there- published analysis). On average, species need fore has to take account of both constraints about 350 day-degrees above the developmental (adversity) and needs (suitability).

Seasonality Unpredictability Variability W extreme C extreme Annual mean Temp. Precip. in W daily mean min. temp., min. temp., precip., mm difference summer, % temp. range, °C °C (extreme °C (extreme (annual snow, cm) W–C,°C of annual (% of mean) max., °C) max., °C) 130 (68) 38.3 73 4.9 (107) –2 (16) –49 (–14) 380 (204) 34.4 58 7.6 (96) –1 (24) –45 (4) 352 (97) 36.9 72 14.5 (75) 2 (40) –46 (9) 850 (219) 31.5 53 11.7 (57) 5 (37) –36 (11) 1551 (380) 19.7 40 9.6 (62) 1 (29) –23 (13) 1347 (3) 19.2 48 11.6 (43) 11 (41) –13 (27) 1142 (0) 3.3 45|| 10.6 23 (34) 20 (31) 2869 (0) 1.5 49 9 (35) 20 (36) 16 (36) 2 (0) 5.5 10†† 7.8 13 (30) 9 (22) (typically April to September). Zone 1, Resolute, NU, Canada (75°N); 2, Iqaluit, NU, Canada (64°N); 3, Saskatoon, SK, America (34°N); 7, Managua, Nicaragua (12°N); 8, Uaupés, Brazil (0°N); 9, Iquique, Chile (20°S). Data from Vowinckel

Signals Frequent or continuous signals can be as- An important feature of habitats is how well sessed regularly. Most major physical cues such they provide to insects signals that can be used as photoperiod, temperature, and moisture are to predict future conditions. Environmental sig- in this category. Signals are easily recognized nals used for this purpose seldom stem directly when sensors are available and when conditions from the resources or conditions that limit sea- change rapidly and evenly between levels that sonal activity, because to avoid adversity or to are well differentiated from one time of the sea- coincide with suitability, insects must generally son to another. Sensors are available for most predict rather than simply monitor seasonal potential cues. Photoperiod is highly recognizable even when the differences from day to day changes. Therefore, except in habitats that are are relatively small, as at some times of year extremely well buffered, such as deeper soil and at lower latitudes, because daylengths layers, proximate rather than ultimate factors change very evenly. Many other signals, such as are used to control seasonal responses. temperature, are less informative because they The most effective signals are reliable, fre- fluctuate widely from day to day. Although av- quent, and recognizable (Danks 1987a, chap. 6). erage temperatures show clear trends over the Signals are reliable when well correlated with longer term, it is usually difficult for insects to the seasons and not subject to short-term noise. integrate this information in ways that would Therefore, the cue of photoperiod, which is as- allow a timely seasonal response. sociated with invariable astronomical events, is Beyond intrinsic elements of the signals the single most reliable environmental signal. themselves, availability or visibility as influ- Thermoperiod is driven largely by the same enced by the insect’s habitat determines their events and shares some of the same features. value for predicting seasonal change. For exam- Food quality is often closely tied to the seasons. ple, the great intrinsic reliability, frequency, and Many other factors, including temperature level recognizability of photoperiod are negated if and most biotic factors, are less reliable. species live in very dark places (such as the soil

and inside some plant tissues) where signals cannot be detected even by sensors with very low thresholds. In essence, insect responses are usually controlled by signals that provide information meaningful for a particular habitat. Conse- quently, for example, photoperiod is not used at the highest latitudes because temperature varies environmental signals correlates always) close to 0 °C and plays a dominant role there, Adjustments of timing using Energy use and other Energy storage Size and time (but not so that even if changes in light intensity or solar elevation could be detected above the Arctic Circle in summer, the seasonal information these cues provide is less relevant than current temperature (e.g., Danks and Oliver 1972b). Likewise, in some circumstances species from deserts with intermittent rainfall would be expected to use moisture, humidity, or food cues

etc. because those factors would most likely indi- cate suitable windows for development. As- sessing habitat features for a given species in parallel with the characteristics of signals and their availability suggests what factors should

; tolerance of or resistance to be tested for potential roles as seasonal signals.

etc. Nevertheless, many insect species make small adjustments in their responses to main factors such as photoperiod by using other signals too (see below). Taking account of additional factors evidently has adaptive value, so testing a phenological and reproductive patterns;and diapause other controls aggregation, cold, dryness, food limitation, microhabitats interactions hinder assessment relatively wide range of conditions is usually Developmental patterns including different stages; Host-plant switches; construction of shelters, wise.

Elements of the response Insects respond to seasonal adversity and habitats that are intermittently favourable for development and reproduction in many different ways, as summarized in Table 2. Spatial differences in conditions are met by long-distance and short-distance movement. Temporal variations in favourability are met by specific patterns of timing of life-cycle components. Other year-to-year differences modification; resistance to adversity adaptations serve to exploit resources and to

Differential resource use; habitat modify or resist the environmental limitations. However, because these many elements may make opposing demands and it is not possible to optimize or maximize every feature simultaneously when resources are finite, trade-offs among various components of the response are usually required. The sets of responses in habitats that have extreme cold, dryness, salinity, or other challenges are especially instructive. Essential elements of seasonal responses. Spatial framework

suitability of environments The simplest way for insects to avoid or co- Temporal differencesAvailability of resources and Life-cycle timing; response to Spatial differences Movement to less severe placesCombined elements Migration; choice of overwintering habitats and Trade-offs Many trade-offs, but multiple rather than one-to-one Table 2. Seasonal constraint Sample response Sample actionincide with given conditions is to choose Sample correlate among

© 2007 Entomological Society of Canada Danks 7 available habitats through movement or specific ones, may allow winter development that would selection. These responses occur on a wide not be feasible otherwise (e.g., Takafuji 1994; range of scales, although small-scale choices Ohashi et al. 2005). are more prevalent than long-distance move- At the smallest scale, many species not only ments. Moreover, movements even at the select microhabitats but also use adaptive be- largest scale end by targeting specific haviours, such as basking, body orientation, or microhabitats, even though responses vary in hiding, especially for thermoregulation; many how many steps and what time or distance is species maintain body temperature within a rel- involved in displacements towards habitats suit- atively narrow range, and finely tuned responses able for development or overwintering. For ex- have been reported (Heinrich 1981, 1993). As ample, the long fall migration of monarch might be expected, most behavioural elements butterflies (Danaus plexippus (Linn.)) (Nym- are adapted locally (Samietz et al. 2005). Allied phalidae) (Brower 1995, 1996) takes them to to these responses are melanism or dark certain trees in certain forested habitats that colouration, which helps absorb solar heat, and offer favourable conditions for overwintering hairiness, which helps retain it (Danks 1981; (Leong 1990; Brower et al. 2002). Adult Baetis Gross et al. 2004). mayflies (Ephemeroptera: Baetidae) disperse from their sites of emergence and oviposit Temporal framework elsewhere in microsites preferred for Insect life cycles consist of stages with dif- oviposition, but the subsequent survival of ferent prominence and with different potentials larvae — and hence the emergence of adults in for activity, resistance, and so on (Danks the new areas — is affected by independent 2000c). These stages are timed according to a processes operating at the local level that are number of general patterns. The timing, espe- different from the influences on adults and their cially for adults, can be described in terms of oviposition in the previous generation phenology, but phenological variables are sur- (Peckarsky et al. 2000). prisingly diverse and may be combined in dif- Lady beetles and noctuid moths may fly con- ferent ways. siderable distances from the lowland habitats Typical metamorphosis includes stages that where they develop, but then choose specific are immobile (eggs, or eggs and pupae), stages aestivation shelters in which to aggregate (e.g., that feed (larvae, or larvae and adults), and Oku 1983). Most other species overwinter rela- stages that reproduce (adults). Delays or tively close to their feeding habitats, but again dormancies are interpolated into many life cy- they first move to suitable general habitats, for cles (for sample reviews see Tauber et al. 1986; example from fields to field edges or wood- Danks 1987a). Although dormancy is common lands, then enter microhabitats chosen on the in immobile stages, as might be expected, it is basis of temperature, light, moisture, touch, and known in any stage and indeed in insects as a other factors (review by Danks 1991b; and see whole appears to be more prevalent in larvae, Nalepa et al. 2005). Such a process parallels which last the longest in most groups except other chains of behaviour in insects, such as beetles. Seeking of food resources, as well as dispersal, then landing, then host selection in wider dispersal, is most common in winged aphids (Powell et al. 2006) and components of adults but also is common in larvae. The dura- habitat selection and then host selection in para- tions of activity and dormancy and the tendency sitoids (Vinson 1976). Viewing seasonal move- to be dormant also reflect phylogeny. Thus, the ments as a series of steps (such as energy diapause stage tends to be the same within gen- acquisition, long-distance movement, habitat era and to some degree within families (Danks selection, and microhabitat selection) helps to 1987a). For example, typical Orthoptera identify logical components for experimental overwinter as eggs, chironomids as larvae, investigation and analysis. sarcophagids as pupae, and drosophilids as Extensive flight and the diapause that accom- adults. In the many families of beetles in which panies both long-distance and short-distance the adult is long-lived and feeds extensively, movement to escape adversity usually depend adults usually overwinter (Danks 1987a), as in on the buildup of energy stores, typically in the coccinellids (Hodek 1973). Major feeding form of lipids (information for many species is stages — larvae in most groups — are typically listed by Danks 1987a). In milder climates, prolonged, but in species that eat ephemeral favourable microhabitats, including artificial foods such as dung, carrion, and fungal fruiting

© 2007 Entomological Society of Canada 8 Can. Entomol. Vol. 139, 2007 bodies, the larval stage is much abbreviated and Fig. 1. Sample stylized phenological patterns (solid then ordinarily is followed by prepupal or pu- lines) with cumulative equivalents (dashed lines, pal, and rarely by adult, dormancy. shown at a different scale). (A) Unimodal, narrow Different stages also have different abilities normal. (B) Unimodal, wide normal. (C) Unimodal, to withstand severe conditions. Dormant stages skewed. (D) Irregular. (E) Bimodal, equal. often require resistance. Such resistance is fa- (F) Multimodal, skewed. For additional information voured in the resting stages of metamorphosis see text. by the fact that in most species those stages have evolved some additional level of mechani- A cal protection, because physical damage accu- mulates and cannot be repaired in immobile individuals. Protection includes the coverings of eggs and the cocoons of pupae (Danks 2002a, and see below). Many dormant, fully fed larvae B or prepupae (Danks 1987a, Table 11) also resist adverse conditions inside cocoons or similar structures prior to metamorphosis to the pupa, for example in many Hymenoptera. Other characteristics reflect the fact that the timing by which suitable resources can be ex- C ploited is easier in some stages than in others. Many species deposit eggs near buds, overwinter as partly grown larvae, or metamorphose in spring and thereby enter a key feeding stage when succulent new plant growth is available D (e.g., Masaki 1980). The timing of reproductive activity also accords precisely with the availability of suitable habitats. For example, many species are dormant in the stage (e.g., pupa) im- mediately preceding reproduction, allowing rapid oviposition soon after emergence in the E spring. This tendency is especially clear in habitats with an abbreviated growing season, where “spring species” (Corbet 1964a) predominate. Finally, some species have complex life cycles with multiple periods of activity, reproduc- F tion, or dormancy or multiple stages that can enter dormancy. These integrated systems are discussed in a later section. The seasonal occurrence of stages (phenology), including the temporal pattern of adult emergence, can be characterized by features such as the onset of emergence, its duration, conditions are fully suitable no individual can the synchrony of individuals, any skew from develop much faster than the norm. However, in normality, and variations including irregulari- other instances the skew is adaptive, with rela- ties and modalities. Easiest to describe are the tively small but significant numbers of late phenological patterns of species with normally emergents providing insurance against catastro- distributed emergence that takes place over a phes that might befall the main population (risk short period (Fig. 1A) or over a longer interval spreading; see Types of variation below). (Fig. 1B). Irregular phenology (Fig. 1D) arises by more Other species have more complex patterns. than one route. Emergence highly dependent on For example, skew (Fig. 1C) is common, giving weather that intermittently falls below the tem- a tail after the main distribution. Often it reflects perature threshold for emergence results in ir- only the fact that some individuals can be de- regular recruitment of adults. Similar patterns layed by local conditions, whereas even when are shown by traps that rely on activity

© 2007 Entomological Society of Canada Danks 9 influenced by weather. Alternatively, emer- Resources and limitations gence in individual microhabitats might be nor- In addition to spatial and temporal coinci- mally distributed, but sections of the population dence, adaptations that facilitate the acquisition in habitats with different conditions emerge at of resources include adjustments of metabolism slightly different times. Combined emergence or activity to enhance development and repro- by individuals in different microclimates can duction, in response to physical conditions or therefore give an irregular pattern (Baker food. At the same time, environmental limita- 1980). In ponds with different mean tempera- tions may prevent normal growth and develop- tures, the same species of aquatic insects ment, and many other adaptations serve to emerge at different times (Danks and Oliver modify local conditions or to resist adversity. 1972a; Corbet and Danks 1973). Moreover, trade-offs balance allocations for dif- Bimodal emergence (Fig. 1E) arises in sev- ferent purposes when resources are limited. eral ways. Separate generations give separate peaks. In many species, developmental deci- Modification of adverse conditions sions (see Control and integration below) accel- Many species actively modify local conditions erate emergence or allow emergence or activity to reduce the impact of adverse seasons, as op- under one condition but retard or prevent it in posed to simply seeking out favourable micro- members of the same cohort under another, pro- sites. These modifications include excavating ducing phenological peaks separated by an un- substrates, constructing shelters, inducing re- suitable season, for example in spring and fall sponses in plants or hosts, and aggregating (in- (cf. Masaki 1980, Fig. 1) or in successive years cluding sociality), as well as modifications made (cohort splitting: e.g., Pritchard 1979; Danks by parents that improve conditions for their pro- geny (reviews by Danks 2002a, 2004b). 1992; Kiss and Samu 2005). Multimodal patterns have several causes too, but of particular Many insects dig into the soil for overwintering, the chamber often strengthened by a interest are skewed patterns (Fig. 1F), such as silk lining. There they are buffered against win- prolonged diapause between years, that — like ter temperatures. Other species overwinter in genetically programmed bimodal patterns — less robust but still protective substrates, such appear to be a way of spreading risk (see Types as plant stems. Excavations also protect against of variation below). The various emergence pat- dry conditions, and some species adjust the terns shown in Figure 1 are paralleled by pat- depth and location of burrows according to des- terns of oviposition after emergence, with the iccation stress (e.g., Rasa 1999). Seasonal added possibility of delayed onset. flooding is offset by a resin lining in nests of Careful measurements and analyses are re- some bees (Roubik and Michener 1980). quired to identify the different patterns. Impor- Some species that eat leaves construct shel- tant information about life cycles and their ters during feeding, especially by tying leaves relationship to natural environments may be together with silk. They include both solitary missed if experiments are too short, observations and communal species. In aquatic habitats, shel- are too limited, or data are improperly grouped ters such as the cocoons of chironomid larvae (Danks 2000c). Also important is the variability and the cases of caddisfly larvae typically are of these parameters from one year to the next. made from saliva and material incorporated Warm, cold, or dry seasons may change the pat- from the substrate. tern of emergence or advance or delay its onset, The most durable cocoons are made by dor- often considerably, for example by 10 days for mant stages. Indeed, overwintering generations mosquitoes in the high Arctic (Corbet and Danks normally construct more robust cocoons with 1973) and by one month for black flies at the thicker walls than do intervening nondormant tree line (Ide et al. 1958). Moreover, the retard- generations of the same species (sample species ing or accelerating effect of a given season is not are listed by Danks 1987a, Table 6). These co- the same for all species. Winter snow accumula- coons provide mechanical protection not just tions and cool or cloudy weather during the against abrasion but also against more severe spring thaw do not affect low-lying aquatic habi- stresses (Danks 1971b, 2004b). The cocoons may tats in the same way as dry elevated habitats act as a humidity buffer (e.g., Tagawa 1996), pro- blown free of snow. Assessing the significance tect against water (Sagné and Canard 1984), or of phenological patterns may thus require several stop ice from reaching the body surface, prevent- years of data from natural habitats. ing freezing by inoculation (Sakagami et al.

1985). Although most cocoons have limited ef- well as to ice scour, spring spates, floods, and fects on temperature, some darkly coloured or other extremes or disturbances (e.g., Mendl and specialized cocoons absorb solar heat and thus Müller 1978; Clifford et al. 1979; Lytle 2002; accelerate development (Kevan et al. 1982; Lyon Prowse and Culp 2003). However, information and Cartar 1996). Cocoons and other shelters also is most abundant about how insects withstand deter many generalist predators during the active cold, dryness (often with high temperatures), season (Dillon 1985; Gross 1993). and lack of food. The galls induced seasonally by insects on plants also protect against some generalist ene- Cold mies, and they give mechanical protection, des- Insects survive the cold of winter by a wide iccation resistance, and so on (Danks 2004b, array of adaptations that have been reviewed pp. 14–15). Some parallel benefits arise through many times (for recent updates and salient ref- use or modification by parasitoids of host struc- erences see Bale 2002; Danks 2005). Elements ture or behaviour (Hippa and Koponen 1984; of these responses are shown in Table 3. Horton and Moore 1993). Insects can be injured at low temperatures Some but by no means all aggregations serve above 0 °C (“chilling injury”) — see Turnock and to increase temperature (Benton and Crump Fields (2005) and references cited therein. Injury 1979; Klok and Chown 1999) and reduce water from cold appears to be associated with a break- loss (Yoder et al. 1992a). Some reduce predation down of membrane structure and membrane-based especially by reinforcing aposomatic colouration ion gradients (Ramløv 2000; Košt’ál et al. 2004; or chemical repellents (Vulinec 1990). A few Zachariassen et al. 2004a); compromised pro- condition the food (e.g., Marchenko and Vino- tein structure and enzyme function have also gradova 1984) or overwhelm host defences been suggested. Corresponding adaptations to (Grégoire 1985) and thus accelerate develop- low temperatures, including temperatures below ment. The most striking benefits of aggregation 0 °C, include modification in the saturation of are seen in colonies of social insects able not membrane fatty acids to maintain function at only to construct a protective nest but also to lower temperatures (e.g., Bennett et al. 1997; condition internal temperature, moisture, food Košt’ál and Šimek 1998; Ohtsu et al. 1998). supply, and so on (Southwick 1987) and to pro- Shock proteins (Craig et al. 1993), produced in tect against predators through structure, repel- response to chilling or heating, are also pre- lents, and coordinated defensive behaviour sumed to protect against low temperatures (Jeanne 1975). (cf. Denlinger et al. 1991; Relina and Gulevsky Finally, substantial seasonal benefits follow 2003); typically they act as molecular cha- from modification by parents of the habitats in perones that help in protein transport, folding which their eggs are deposited and their larvae and unfolding, assembly and disassembly, and develop. Eggs of some species are protected by aggregation processes. Nevertheless, it has placement, concealment, or robust coverings proved difficult to associate the occurrence or such as oothecae (cf. Richards and Davies reduction during cold hardiness or diapause of 1977, p. 321), paralleling the protection af- shock proteins or other molecules (or the up- forded to active stages by their own efforts such regulation or downregulation of responsible as burrowing and cocoon making. Depending genes) with their detailed function (Storey and on the species, protection of eggs in the ovi- Storey 1999), despite many recent studies. In- position site, retention of eggs inside the deed, there are many interspecific differences mother during development, or parental care (compare, for example, Hayward et al. 2005 provided to larvae can prevent ice inoculation, and Tachibana et al. 2005; see also Jung and flooding, and desiccation; reduce predation, Lee 2005; Kayukawa et al. 2005; Michaud and parasitism, and even diseases; and supply food Denlinger 2005) and even differences between resources (Danks 2002a, p. 17). winter diapause and summer diapause in the same species (Chen et al. 2005). Resistance to adversity At temperatures below 0 °C, most species re- Many types of adversity can prevent the ac- main unfrozen because they supercool. Several tivity or threaten the survival of insects. For ex- systems are used in the same or different spe- ample, adaptations are known in response to cies to prevent freezing. Ice formation is most anoxia (Nagell and Brittain 1977; Hoback and likely when molecules can assemble in the ap- Stanley 2001; Hodkinson and Bird 2004) as propriate configuration (that of the ice crystal)

© 2007 Entomological Society of Canada Danks 11 d odes) ); dehydrate passively by readily losing water etc. etc. through the cuticle to surrounding ice other features other substances; some species manufacture multiple solutes Common mechanisms of direct resistance to cold in insects. Indirect methods such as seasonal inactivity, site selection, and cocoon construction are treated elsewhere. Note: Protect membranes or membraneProtect function proteins, enzymes, and other functionsPrevent freezing Lower haemolymph melting pointLower haemolymph freezing point PotentialPrevent Membrane roles inoculative transition freezing of temperature shock loweredReduce proteins by nucleation and changing sites other composition molecules ofEliminate fatty nucleators acids Mask nucleatorsReduce water available for the freezing process ManufactureSurvive of freezing low-molecular-weight solutes, includingLimit glycerol, supercooling other Antifreeze to polyhydric proteins reduce alcohols,Reduce lower impact sugars, the amount of some freezing and freezing point rate eventsProtect (this of Associate membranes action formation water or is of with membrane enhanced iceProtect cell Manufacture function by Some other constituents of glycerol antifreeze functions (“bound nucleating and proteins water”, proteins; otherRapid prevent cuticular molecules) cold ice structure hardening inoculation readily allowingPrevent inoculation recrystallization during Adaptations thaw inModify structural water proteins, status Empty ManufactureDynamic gut low-molecular-weight adjustments cryoprotectants SeeSeasonal above; adjustment also, of protection cryoprotectants provided Nucleators by or association nucleation ofRapid sites various cold masked cryoprotectants hardening by with nucleation membranes Freezing-induced inhibitors change in supercoolingLinkages points with Manufacture diapause of antifreezeSeasonal proteins; adjustment manufacture of of mitochondria specificOngoing recrystallization repairs See inhibitors above (known in Solutes nemat and Freezing antifreeze Enhanced exposure proteins resistance lowers change caused supercooling through by points the brief in winter cooling some in beforehand species some species, changing Unreactive supercooling glassy points states an mediated especially by carbohydrates such as Mitochondria trehalose reduced during winter cold and See inactivity above Diapause is a prerequisite for some elements of cold hardiness in some species Warmer intervals permit injury caused by cold exposures to be repaired in some species Survive chilling Interaction between antifreeze proteins Enhances action Table 3. Mechanism Sample systems or substances

© 2007 Entomological Society of Canada 12 Can. Entomol. Vol. 139, 2007 around a physical nucleus, and indeed in the Zettel 2003). The cold hardiness of several spe- absence of such a nucleus freezing is unlikely cies in extreme environments includes marked until water molecules are moving very slowly dehydration (e.g., Danks 1971b; Ring and at the homogeneous nucleation temperature, Danks 1994; Bennett et al. 2005). which is about –40 °C (Vali 1995). The inci- Some soil organisms with permeable integu- dence of freezing is therefore reduced by elimi- ments, including some earthworms, enchytraeids, nating nucleators. This can be done through and springtails, remain unfrozen by progressive modification of the tissues (as by the design of dehydration through the cuticle to surrounding structural proteins, cf. Zachariassen et al. ice. This loss concentrates solutes in the body 2004b), by eliminating certain molecules (e.g., fluids to a level at which the fluids will not Neven et al. 1986), and by evacuating the gut freeze (Holmstrup and Zachariassen 1996; (because typical ingested food has potent Holmstrup et al. 2002). A similar phenomenon nucleators). Some species may even moult to has been reported for stonefly eggs, which de- eliminate gut nucleators (Worland 2005). hydrate and supercool below –29 °C while sur- Nucleators and nucleation sites can also be rounded by ice (Gehrken and Sømme 1987). masked by inhibitory molecules (cf. Wilson et Another set of insects survives actual ice for- al. 2003). mation in the body. Such freezing-tolerant spe- Supercooling is enhanced too by solutes of cies typically limit the degree of supercooling low molecular weight, chiefly polyhydric alco- because the very rapid ice formation that takes hols and sugars (examples are listed by Lee place in highly supercooled solutions increases 1991 and Ramløv 2000), which can reach multi- the extent of injury compared with slow freez- molar concentrations in overwintering insects. ing. Proteins that ensure nucleation are manufac- These substances lower melting and freezing tured by many freezing-tolerant species (review points by colligative action, so that their effects by Duman 2001; Lundheim 2002). Some other are additive. Many species have more than one freezing-tolerant species survive only if frozen kind of solute, for example both glycerol and by inoculation (review by Duman et al. 1991; sorbitol. Riihimaa 1996), suggesting that they lack ice Larger antifreeze proteins (review by Duman nucleators but that the cuticular structure offers 2001) lower the freezing point but not the melt- no resistance to inoculation. Low-molecular- ing point by inhibiting ice formation (cf. weight cryoprotectants in freezing-tolerant spe- Kristiansen and Zachariassen 2005). This action cies serve to decrease the amount of ice formed is enhanced by other antifreeze proteins to- at a given temperature and to slow its rate of for- gether with certain solutes of low molecular mation (Ramløv 2000). Relationships of tissue weight (e.g.,Liet al. 1998; Duman 2002; freezing with anoxia have also been considered, Duman and Serianni 2002; Wang and Duman because freezing impedes oxygen delivery (e.g., 2005, 2006). Some of the antifreeze proteins Morin et al. 2005). found in superficial tissues or around the gut Freezing tolerance is associated in some spe- appear to prevent inoculation by ice (Olsen et cies with a change in the state of water to form a al. 1998). Antifreeze proteins are also known to homogeneous glass, which prevents all molecu- inhibit recrystallization of ice during post- lar diffusion and reactions and thus inhibits met- freezing temperature changes or thawing abolic processes as well as solute crystallization. (Duman 2001). Cells can be injured by such re- Glasses form, typically by dehydration, in the organizations of ice crystals and not only by the presence of certain carbohydrates at high con- initial formation of ice. At least some inverte- centration. Trehalose is the best known glass for- brates have specific recrystallization inhibitors, mer, mediating glasses at relatively high and which are smaller than typical antifreeze pro- ecologically relevant temperatures (Ring and teins (Ramløv et al. 1996). Danks 1998; Danks 2000a). The freezing process depends on the supply of Also known to enhance cold hardiness is water molecules, and so closer association of rapid cold hardening, typically in active stages: water with biological molecules or surfaces re- relatively brief exposures to mild cold enhance duces the likelihood of freezing. Such changes subsequent resistance to more severe cold are responsible for significant winter reductions (overview by Danks 2005). Rapid cold harden- in the amount of “freezable water” or “osmoti- ing occurs in a range of taxa. Moreover, it can cally inactive water”, also termed “bound water” give additional protection in cold-acclimated or (Block 2002; Wolfe et al. 2002; Block and winter individuals (Powell and Bale 2005 for an

© 2007 Entomological Society of Canada Danks 13 aphid) or additional freezing tolerance (Lee et diapause program are prerequisites for some as- al. 2006a for an antarctic midge). Production of pects of cold hardiness (Denlinger 1991; shock proteins and cryoprotectants is associated Šlachta et al. 2002; Hodkova and Hodek 2004; with rapid cold hardening in some species (Qin review by Danks 2005). Susceptibility to cold et al. 2005; Yoder et al. 2006a) but not in oth- shock may also depend on diapause status (Pitts ers (Lee et al. 2006a). Changes in membrane and Wall 2006). lipid composition or fluidity have also been re- These many differences among species are ported (Overgaard et al. 2005; Lee et al. not surprising. Different species have evolved 2006b). These differences suggest that rapid different life-cycle programs, cold hardiness, cold hardening involves several different pro- and other adaptations. For example, antifreeze cesses, but we do not know their functioning in proteins appear to have evolved independently detail. in collembolans and insects (Graham and Davies Evidence is also accumulating as to how other 2005). Because habitat and water relations as elements and pathways are involved in cold har- well as temperatures affect overwintering con- diness, such as cholesterol (Yi and Lee 2005) ditions in a complex way, conclusions about the and membrane transport of cryoprotectants and evolution of different types of cold hardiness water (Izumi et al. 2006), although again the are not well developed (Danks 2005), although, details remain to be worked out. Nor are some as might be expected, freezing tolerance is other potentially allied responses understood. more prevalent in insects from colder climates For example, recovery from chill coma is com- (Turnock and Fields 2005). plex (Macdonald et al. 2004). Cold hardening Other dynamic aspects of cold hardiness that that reduces mortality from cold does not re- have been reported but as yet are little under- duce chill-coma recovery times (Rako and stood include mitochondrial degradation during Hoffmann 2006). However, rapid cold harden- winter (Kukal et al. 1989; Levin et al. 2003), ing may reduce the chill-coma temperature the effects of fluctuating temperatures on sur- (Shreve et al. 2004). vival, interactions between antifreeze com- A major conclusion that can now be drawn pounds that enhance their collective action (see about insect cold hardiness is that many of its above), and changes in supercooling points on a features are dynamic (Danks 2005). Cold hardi- daily basis (Worland and Convey 2001; Sinclair ness is not a static condition instituted for the et al. 2003). Ecological interactions figure in winter, but a series of complex developmental many of these adaptations. For example, insects and metabolic patterns. For example, some spe- may select low-temperature habitats when there cies adjust cryoprotectant levels in fall and are frequent freeze–thaw transitions in order to spring and even during winter (Baust and allow a cold-hardy state to be maintained (Hay- Nishino 1991). Cold hardiness levels vary both ward et al. 2003). Understanding all of these over the long time frame of winter and over elements therefore depends on integrating much shorter intervals (cf. rapid cold harden- knowledge about the specific ecophysiological ing). For example, the type of cold hardiness adaptations with knowledge of patterns in the may change between chilling-susceptibility and environmental challenges they have been se- freezing-susceptibility according to life stage lected to overcome. and acclimation (Carrillo et al. 2005). Freezing exposure lowers the supercooling point of indi- Dryness viduals in subsequent exposures in a few spe- Many natural systems are seasonally dry, es- cies (Bale et al. 2000, 2001; Brown et al. pecially in summer, and droughts can have sig- 2004). The effects of cold across different tem- nificant and long-term effects on ecosystems perature ranges and with different times of ex- (Humphries and Baldwin 2003; Lake 2003). posure interact, for both chilling and freezing Even many winter habitats are very dry, and ad- injury, and there is some repair of cold injury aptations to cold and desiccation overlap (Ring during warmer spells (Nedvd et al. 1998; and Danks 1994, 1998; see also Worland and Renault et al. 2004; review by Turnock and Block 2003; Williams et al. 2004). Fields 2005). Diapause is linked to cold hardi- Several different adaptations enhance survival ness to different degrees. Even here, the rela- when water is in short supply, especially in dor- tionships are complex and diapause and cold mant individuals that cannot move to find it (re- hardiness are not simply codependent. Rather, view by Danks 2000a). These adaptations serve in several species at least some aspects of the to limit water loss, acquire water, or tolerate

© 2007 Entomological Society of Canada 14 Can. Entomol. Vol. 139, 2007 water loss, as summarized in Table 4. Such different taxa. In particular, the osmotically ac- characteristics can be selected relatively rapidly tive substances in advanced endopterygote in- (Chown and Klok 2003a). sects are small organic molecules (such as A main suite of adaptations in dry environ- amino acids), and sodium and chloride play rel- ments limits the loss of body water, which is a atively small roles (review by Hadley 1994). function of body size because the surface to These different systems must influence the volume ratio is larger in small individuals. Inac- routes and types of damage to cells during des- tivity during dormancy conserves water (Benoit iccation. Some species, especially while dor- et al. 2005). Many species reduce cuticular per- mant, allow haemolymph concentrations of meability through thick sclerotization, often osmoeffectors to increase greatly during dehy- with an impermeable surface wax layer (review dration, but other species osmoregulate, typi- by Edney 1977; Alarie 1998), which is much cally by removing ions from the haemolymph thicker during dormancy (Danks 1987a,p.23; and sequestering them in the fat body (Hadley Yoder et al. 1992b, 1995; Kaneko and Katagiri 1994; Bjerke and Zachariassen 1997). 2004; Nelson and Lee 2004). The level of satu- Active individuals usually can acquire water ration of epicuticular hydrocarbons is lower in relatively easily, by drinking, by eating moist diapause individuals of some species (Kaneko food, and perhaps by metabolizing suitable and Katagiri 2004). Spiracular losses through food (review by Hadley 1994). Both non- respiration are also greatly reduced by the low- dormant and dormant individuals of several ered metabolism of diapause individuals (e.g., taxa have structures to absorb liquid water (e.g., Williams and Lee 2005). Structural modifica- egg hydropyles), and moreover structural and tions such as sunken and protected spiracles or physiological adaptations are used by some spe- spiracles opening into subelytral chambers re- cies to acquire water. The cuticle of some duce such losses too (Greenslade 1981; Draney desert beetles condenses water, which runs 1993; Hadley 1994; Byrne and Duncan 2003). down the tilted body to the mouth (Parker and Cyclical opening of the spiracles (especially in Lawrence 2001). Special structures and hygro- diapause individuals) is also supposed to reduce scopic secretions have evolved in many differ- water loss by keeping spiracles closed except ent groups of insects and arachnids that allow for short bursts to allow gas exchange (e.g., water to be absorbed down to very low partial Kanwisher 1966; many subsequent papers; pressures (Knülle 1984), and even from air well Jõgar et al. 2004), although there has been dis- below saturation. These secretions typically cussion of whether it actually evolved for that rely on high concentrations of potassium ions purpose or instead stemmed from the hypoxic for rectal absorption in insects using structures and hypercapnic environments characteristic of derived from the excretory system. The hygro- underground burrows, where it would favour scopic fluid that facilitates oral absorption in carbon dioxide release (Lighton 1996, 1998). other insects and mites may derive from the sal- However, discontinuous gas exchange does not ivary glands (review by Hadley 1994). appear to favour release of carbon dioxide rela- In the springtail Folsomia candida (Willem) tive to loss of water (Gibbs and Johnson 2004), (Isotomidae), water can be absorbed through it has evolved independently several times, and the permeable cuticle following a rapid increase it does conserve water in dormant individuals in osmolytes such as myoinositol and glucose and those from extreme habitats (see below). (Bayley and Holmstrup 1999). The possibility Such a system is feasible only because tracheal that insects can metabolize water from stored oxygen continues to be available in insects reserves has often been suggested (compare down to very low partial pressures. Water is Dautel 1999 for ticks), but the details of such a also conserved by excretion with minimal use process and the relationships between energy of water (Edney 1977). and water production are not well understood. Water in the body is partly controlled by sol- Finally, a few species tolerate loss of water, utes, which increase the osmotic pressure and reducing to as little as 30% of the original fresh lower the vapour pressure, helping to resist des- weight (review by Edney 1977). Tolerating wa- iccation. Solutes also enable transfer of water ter loss is normally effective only in the short among compartments within the body: active term. High initial water content favours survival transport of ions causes water to follow. So- when drying conditions are not extreme (e.g., dium and chloride are the major inorganic ions, Miller 1968). In response to drying, water may but others participate to different degrees in be moved among body compartments by active

© 2007 Entomological Society of Canada Danks 15 ). a enhance dehydration resistance pressure cycles also may conserve water biochemical adaptations permit tissues to survive when water is withdrawn notably trehalose Biochemical adjustments alter the relationships (incuding vapour pressure) of body water fractions in ways that etc. Common mechanisms of direct resistance to dehydration in insects (after Danks 2000 Indirect methods such as seasonal inactivity, site selection, and cocoon construction are treated elsewhere. Note: Increase sizeReduce activitySeal cuticleEvolve modified spiraclesClose spiraclesSequester solutes, osmoregulate, Acquire water Sunken spiraclesDrink protected Larger by Inactivity insects hairs reducesEat have and respiratory food a other loss containing lower structures surface/volume water reduceAbsorb ratio water liquid and loss water so during Additional lose respiration;Absorb or water subspiracular or thicker more tracheal condense wax slowly water coatings thanMetabolize vapour reduce small water cuticular ones from Spiracular permeability food closingMetabolize inhibits water spiracular from water stored loss; reserves cyclicTolerate gas loss exchange Some Normally may species only reduce haveMaintain As active specific water high above; individuals structural loss the water eat and in relative contentSurvive physiological contribution dormant low of adaptations insects water energy to content and extract Metabolism water water Some produces from vapour species water, from different but have substrates air it specific varies structures is to seldom absorb known that Normally water, including such only egg metabolism active hydropyles individuals is and drink linked Greater the water to losses ventral or water can tubes solutions balance be of tolerated springtails from Compartmentalizing a water, higher regulating starting osmotic point effects, making more water osmotically inactive, and other Limit loss Enter anhydrobiosis Metabolism ceases after a period of preparation: complex sequence of adaptations including protective substances, Table 4. Mechanism Sample systems or substances

© 2007 Entomological Society of Canada 16 Can. Entomol. Vol. 139, 2007 transport of ions, as well as by the osmotic range of food plants rather than only one (re- changes induced directly by drying. view by Danks 1987b). Moreover, many arctic A few species can tolerate extreme drying to species are generalist saprophages or predators less than 5% water content when they enter an that can survive in areas where less widespread anhydrobiotic state. Anhydrobiosis is known in foods are restricted (Danks 1981, 1990, etc.). several small invertebrates such as crustaceans, Many species prolong their development if rotifers, tardigrades, and nematodes, in spring- food is limited or of poor quality, and others tails, and in the chironomid midge Polypedilum delay reproduction in the absence of suitable vanderplanki (Hinton) (Greenslade 1981; adult food. For example, typical anautogenous Crowe et al. 1992; Watanabe 2006). The adap- biting flies develop eggs only after they acquire tations required are highly specific, involving a blood meal. relatively slow water loss, which is often fa- Starvation can be withstood by reducing me- voured by behaviour or surface changes, ac- tabolism. Of course, species in diapause do this, companied by a cascade of biochemical and but also predators such as spiders almost halve other adjustments that require metabolic activ- their metabolic rates without dormancy when ity, including trehalose production (Ring and starved, and may switch to metabolizing fat Danks 1994; Kikawada et al. 2005). However, (e.g., Anderson 1974; Tanaka and Itô 1982). in P. vanderplanki isolated fat body tissues Such abilities are also well developed in species manufacture trehalose and can enter the an- such as ticks and bugs that feed on vertebrate hydrobiotic state without any central control blood (e.g., Moreira and Spata 2002). The high (Watanabe et al. 2005). Once in anhydrobiosis, arctic moth Gynaephora groenlandica (Wocke) the organisms are remarkably resistant to both (Lymantriidae) also adjusts metabolism accord- natural and artificial extreme conditions ing to food supply (Bennett et al. 1999). Such (Jönsson 2003), and the time spent in this state species can survive for many months without is not counted as part of the developmental pro- food. gram (Ricci and Covino 2005). The various adaptations for dehydration re- A major route for withstanding starvation is sistance, including anhydrobiosis, confirm the the accumulation of extensive reserves, typically dynamic nature of water relations in insects lipids stored in the fat body, to supply energy in from dry environments. Sequential or reversible the absence of feeding. Some adult insects can- adjustments of water status can be integrated not feed, and any that are not short-lived then through absorption or osmoeffectors, for exam- rely on food stores carried through from the lar- ple. Water in insects is in several different states val stage. There is a great deal of information that are largely or partly interdependent (Danks about starvation resistance and trade-offs be- 2000a). Indeed, as was concluded for cold har- tween stored reserves and other features (in- diness, most adaptations to dry environments cluding cold hardiness, for example) within and appear to reflect ongoing metabolic adjust- among species of Drosophila (e.g., van Herre- ments, not just entry into some sort of inert wege and David 1997; Chippindale et al. 1998; state. Even the unreactive state of anhydrobiosis Hoffmann and Harshman 1999; Hoffmann et al. depends on prior specific metabolic sequences. 2003, 2005a, 2005b), but there has been less analysis of similar phenomena in other species Food limitation of insects. Findings for Drosophila show espe- Survival when food is limited can be en- cially that energy metabolism is complex and hanced by eating what is available rather than a varies among species, so that a range of re- restricted diet, and by tolerating starvation (Ta- sponses to food limitations would be expected ble 5). Many predators change diets seasonally, at the metabolic level, depending on the habi- eating any common species of the right size tats and life styles of different insect species. that they can catch. Some herbivorous species Other metabolic problems may have to be also change food plants in a seasonal pattern; solved by insects that are inactive for very long this is most easily demonstrated when there is a periods in the absence of food. For example, strict seasonal alternation between hosts, as in adults of the shield bug Parastrachia japonensis many aphids that alternate between perennial Scott (Cydnidae) appear to recycle uric acid overwintering hosts and ephemeral summer from the midgut as an amino acid source, by food plants. Many but not all species in chal- means of symbiotic bacteria (Kashima et al. lenging environments such as the Arctic eat a 2006).

Table 5. Common mechanisms of direct resistance to food limitation in insects.

Mechanism Sample systems or substances Use available supplies Widen food range Wide range of food plants Widen habitat Generalized saprophagy in soil habitats Eat what is present Change diet seasonally Tolerate starvation Reduce energy use Prolonged development, delayed reproduction, and other resource allocations Reduce energy requirements Reduced metabolic rate Store reserves Accumulate extensive reserves, especially lipids in fat body Note: Indirect methods such as seasonal inactivity are treated elsewhere.

Trade-offs commodus (Walker) (Gryllidae), more fecund fe- Resources are normally limited, but organ- males exercise greater mate choice (Hunt et al. isms can allocate resources among different traits 2005). Such trade-off decisions can influence to maximize fitness. The differential allocation subsequent population dynamics. In the mite of resources — trade-offs — gives insight into Sancassania berlesei (Michael) (Acaridae), the how life cycles are constructed and what types level of maternal investment (through an egg of life cycles are possible in particular circum- number – egg protein trade-off mediated by the stances. Genetic programmes can incorporate mother’s age as well as her food supply) influ- set trade-offs (such as the allocation between ences how populations will develop over several energy stored in eggs and energy devoted to generations because of ongoing competitive ef- flight), and also trade-offs can change within a fects (Benton et al. 2005). season in response to current conditions, by Trade-offs can be made effectively only phenotypic plasticity. For example, females of when there is some stability of the resources the bean weevil Bruchidius dorsalis (Fahraeus) being acquired, and they tend to be obscured (Coleoptera: Bruchidae) lay larger eggs when when conditions are very variable (e.g., their offspring will encounter harder seeds, pro- Messina and Slade 1999; Messina and Fry ducing larger larvae that can drill farther into 2003). Conversely, when food reserves are es- the seeds (Takakura 2004). Of course, both ge- pecially abundant, the trade-offs normally re- netic and environmental factors are involved; in quired may not be necessary, so that trade-offs one study of stress resistance in Drosophila, between size and time are not observed (e.g., differences among environmental conditions were Cortese et al. 2003; Wissinger et al. 2004). one-and-a-half times greater than the heritable Even when limitations make some sort of trade- (genetic) ones (Hoffmann et al. 2005a). The off essential, the features expected to trade off main features of trade-offs are summarized in or to coincide may instead be independent of Table 6. one another (though they may trade off with The assessment of trade-offs is by no means other elements). For example, instances of inde- simple, for several reasons (cf. Danks 1994, pendence between offspring production and 2002b, 2006b). Resources that are never surplus reproductive investment (Frankino and Juliano (“constraints”) cannot be traded off (discussion 1999), resistance to heat and resistance to cold by Danks 2002b, pp. 133–134). Allocations es- (Hercus et al. 2000), and time and size (Nylin sential to survival are protected, so that they are 1994; Klingenberg and Spence 1997; Vorburger unlikely to be traded off. Development that is 2005) are known. Some of these disconnects re- not modified in response to circumstances is said flect the fact that the components potentially to be canalized; for example, growth of some trading off do not have equivalent weight. Size blepharicerids is insensitive to temperature may modify and even overwhelm other trade- changes (Frutiger and Buergisser 2002). Even offs (Morse and Stephens 1996; Roff et al. behavioural traits may depend on the conditions 2002). In particular, multiple factors trade off experienced, integrating the availability of re- simultaneously, with complex reaction norms sources with many subsequent life-cycle fea- (e.g., Stillwell and Fox 2005; Fischer et al. tures. For example, in the cricket Teleogryllus 2006), and the simple one-to-one relationship

© 2007 Entomological Society of Canada 18 Can. Entomol. Vol. 139, 2007 or rate, growth rate, survival, fecundity, and longevity pathways resistance to heat,pressure, cold, wing and morph otherand or adverse conditions, late dispersal, predator fitness, reproductive pattern, eggduration early size versus versus post-diapause egg fitness number, and diapause not usually possible Customarily emphasized are size or weight, developmental time Trade-offs are effected through various metabolic and other Growth rate is insensitive to temperature Other elements include competitive ability, wing morph, All of the components listed above are in dynamic balance Limited food determines final size directly Growth rate is not routinely maximized most trade-offs relate in many different ways inflexible traded off (unlike typical 1:1 laboratory tests) cannot be traded off not necessarily ateven their under maximum temporal levels, constraints Many elements are integrated at once Developmental and reproductive traits are trade-offs maximum EnergyCanalization Energy Development isOther may the elements be common canalized limiting to currency be Many other resources potentially can be BothSimultaneous long-distance dispersal and immediate high fecundity are Traits below The main features of trade-offs. Complexity Major elements Certain elements are especially important in Flexibility Many pathways The factors in a potential trade-off can Limits Constraints Resources that are only at minimum levels Table 6. Feature Components Details Examples

© 2007 Entomological Society of Canada Danks 19 between a pair of factors selected for study in therefore is one key to interpreting trade-offs. the laboratory and seen to be traded off may not Useful insights might come too from study of represent a natural situation. Most attention has physiological and endocrine regulation of the been paid to key measures of fitness such as responses (cf. Davidowitz et al. 2005; Zera duration or rate of growth or development and 2005). Another key need is to discover how the egg production or fecundity, which have been ability to respond appropriately through pheno- examined especially in relation to size, resis- typic plasticity is maintained (Nylin and tance to adverse conditions, competitive ability, Gotthard 1998; Danks 2006a). Long-term study wing morph, and fitness elsewhere in the life of genetic mechanisms and variations therefore cycle, but there are many other potential inter- is required too (see Types of variation below). actions. For example, developmental rate and size can influence immune function (Rantala Responses in extreme habitats and Roff 2005). Therefore, studies of multiple Habitats in which conditions become unpre- traits reveal complex correlations, some of them dictably extreme as well as seasonally extreme unexpected (Miyatake 1998). Developmental offer particular sets of challenges, and it is in- time in Drosophila increased in individuals se- structive to see how insects cope with them. lected for longevity at high temperatures, but de- Such environments include regions such as the creased when cold-stress-selected lines were Arctic and deserts as well as individual habitats selected for longevity at low temperatures that are temporary or saline. Moreover, some (Norry and Loeschcke 2002). Some trade-offs environmental elements are shared among chal- or correlations, such as stress resistance and lenging habitats. For example, the high Arctic longevity or developmental rate and growth is very dry and therefore is a cold desert, bodies rate, break down after prolonged laboratory se- of water in desert habitats are often temporary, lection (Archer et al. 2003; Phelan et al. 2003). and in deserts both terrestrial and aquatic habi- The complex and dynamic nature of trade- tats may be saline because of evaporation. offs now revealed (Danks 1994; Nylin and The adaptations of arctic and subarctic in- Gotthard 1998) is helpful for interpreting life sects to the long cold winters, short cool sum- cycles. “Stressful” situations force trade-offs, mers, and variability of the region have been and stress can come from the limitation of sev- reviewed several times (e.g., Downes 1965; eral kinds of resources, including not just en- Danks 1981, 1990, 2004a; Hodkinson 2005b). ergy but also time. When time to complete The severe winters are met by cold hardiness development is limited, for example, trade-offs and habitat choice, as might be expected, but take different forms according to species: re- even so there are unusual cold hardiness adapta- duce developmental time and reduce size; main- tions in some species (Danks 2000b, 2004a), tain developmental time and reduce size; or such as very low supercooling points (Ring increase developmental time and maintain size 1981, 1983), freezing tolerance despite very (references in Danks 2006a). However, in yet low supercooling points (Ring 1982), and freez- other species or circumstances time is not lim- ing tolerance despite an absence of the usual ited, and such trade-offs are not necessary. cryoprotectants (Ring 1981, 1983). Different Moreover, we also know that growth is not rou- species show different patterns of relationship tinely kept at the maximum possible rate between water, freezing, and desiccation (Block (Margraf et al. 2003; Tammaru et al. 2004), de- 2002), but both small cryoprotectants such as spite an expectation derived chiefly from stable, glycerol (Ring 1983) and antifreeze proteins nonseasonal laboratory situations that the net (Duman et al. 2004) are widely distributed. As reproductive rate will be maximized. Instead, might be expected, cold hardiness of some spe- individuals retain some flexibility of growth cies persists year round (e.g., Kukal 1991; rate, a trait that would widen the range of op- Sinclair and Chown 2005a). tions available for dealing with environmental Adaptations to the short cool arctic summer challenges. include activity at low temperatures, selection The recent analysis of trade-offs shows even of warm habitats and microhabitats (e.g., greater complexity than had been envisaged Böcher and Nachman 2001), and melanism and earlier. These complexities stem from the dif- hairiness (review by Danks 1981; Danks et al. ferences among real environments and the ways 1994). Selection of habitats with suitable mois- in which multiple features interact. Understand- ture regimes is also important (Hayward et al. ing environmental features and their variations 2004). Basking behaviour is well developed in

© 2007 Entomological Society of Canada 20 Can. Entomol. Vol. 139, 2007 adults (Kevan and Shorthouse 1970; Kevan regions, and this has been interpreted as buffer- 1975, 1989) and even larvae (Kevan et al. ing populations against change, thus protecting 1982; Kukal 1991) and is enhanced by well-adapted genotypes against rapid responses melanism and hairiness. Hairiness and similar by selection over only a few years that might structures that retain a boundary layer of air prove deleterious over the longer term (Downes also play an important role in resisting desicca- 1965; Danks 1981, 2004a). tion (Bennett et al. 2001). Some biting flies do A number of lessons can be drawn from the not feed on blood (hosts are in short supply or range of adaptations in arctic species. First, the are hard to find) and others do so facultatively species respond to multiple simultaneous influ- only if hosts are available (Corbet 1964b). ences, including interspecific interactions even Some species have abbreviated life cycles in this depauperate zone. For example, there are with relatively rapid development during sum- complex timing and other interactions among mer and reach the same overwintering stage insects and plants (Danks 1987b). Second, suc- each year. For example, high arctic mosquitoes cess can follow from several different routes, overwinter as drying-resistant and freezing- for example both abbreviated and prolonged resistant eggs that hatch early in spring, and life cycles. Third, the key selective forces are subsequent larval and pupal development are not necessarily the most obvious ones. Many rapid (Corbet and Danks 1973). Other species, species choose the habitats that will thaw earli- including those that are large, feed each sum- est, even if that increases their exposure to win- mer and overwinter several times in different ter cold. Some caterpillars overwinter exposed larval stages. Such life cycles can last for many on high arctic ridges (Danks 1981), and high years (Butler 1982; Lantsov 1982; Kukal and arctic mosquitoes deposit eggs only in the sites Kevan 1987; Morewood and Ring 1998; Søvik that will thaw first in spring (Corbet and Danks and Leinaas 2003; Søvik 2004; review by 1975). When the season is very short, therefore, Danks 1981). Slow development may stem not time can be more important than severity. only from cool temperatures as such but from Fourth, life cycles are characterized by both prolonged or repeated exposures to cold, which flexibility and fixity: strict programming is might necessitate repair (Sinclair and Chown needed at some times to ensure that reproduc- 2005b). tion coincides with favourable conditions, and Species with annual or longer life cycles typ- the simple ability to grow whenever it is warm ically emerge early in the year, maximizing the enough is not sufficient (Danks 1999). period for feeding and reproductive activity Finally, microhabitats are especially impor- during the warm season. Many high arctic spe- tant, leading to very small-scale responses. The cies carry this tendency to the extreme, emerg- key influence is insolation, which warms insect ing only if they have completed growth the habitats by as much as 10 or 20 °C above ambi- previous year (“absolute spring species”: Danks ent temperature (Sørenson 1941; Corbet 1972). and Oliver 1972a) and deferring until the next The warmed surface of the ground, plant season any individuals not emerging as early as clumps, and shallow waters are the most impor- possible. Some such responses, as well as life tant habitats for arctic insects. As a result, cycles that include a moult to the next instar cloudiness influences insect habitat tempera- each spring (Danks and Byers 1972; Søvik et tures, so that moisture regimes are important al. 2003), appear to be controlled by diapauses both directly and through their effects on tem- (e.g., Birkemoe and Leinaas 1999). They reflect perature. Indeed, in the northwestern high Arc- strict life-cycle control at critical stages, even if tic, with small islands in an extensive ocean, it flexible behaviour and development are permit- might even be supposed that any effects of cli- ted at other times (Danks 1999). matic warming on insect habitat temperatures A final set of adaptations in arctic species will be more than offset as sea ice melts: the responds to long-term variability such as moisture available from greater expanses of below-average temperatures over several years. open ocean water will lead to increasing cloud Prolonged diapause in some individuals (see cover that blocks the sun (Danks 2004a). below) and deferred emergence in cool years Many adaptations are known in arthropods (Oliver 1968; MacLean 1973) allow part of the inhabiting hot deserts that are characterized by population to avoid a summer season that may high temperatures and extreme dryness, often be unsuitable. In several taxa, parthenogenesis exacerbated by strong winds, sand storms, ab- is more common in the Arctic than in other sence of shade, and impenetrable soils (sample

© 2007 Entomological Society of Canada Danks 21 reviews by Cloudsley-Thompson 1975, 1991, cycles of desert insects are coordinated to the 2001; Crawford 1981; Seely 1989; Costa 1995; conditions, but depending on the species and its Sømme 1995; Heatwole 1996; Punzo 2000; see habitat both rapid or slow development and also adaptations to dryness above). A few spe- multivoltine or univoltine cycles occur (Punzo cies (e.g., leaf miners and gall formers) live in 2000). relatively moist microhabitats (Wiesenborn In any event, insects from deserts respond to 2000), but most species avoid the worst condi- the conditions there in ways that reinforce some tions by sheltering in burrows or crevices dur- of the generalizations drawn from insects in ing the day and emerging only during the arctic habitats. For example, multiple elements cooler night (Henschel 1998). Such temporal of ecology, behaviour, structure, physiology, and spatial restrictions are often enhanced by and development are coordinated. Although endogenous circadian rhythms (e.g., Alpatov et convergent adaptations are common, successful al. 1999). Wider searching activity may be con- development and reproduction can be attained fined to more humid periods (Rasa 1994). Sea- in more than one way, so that desert insects sonal dormancy is common and most species show a range of voltinism, fecundity, and other time reproductive activity with cooler or wetter features. Nevertheless, although adaptations in periods. When these are irregular, individuals such extreme environments are coordinated and of many species hatch, pupate, or emerge in di- often in extreme form, survival in desert in- rect response to rainfall (cf. Denlinger 1986 for sects, as in arctic ones, depends not on striking tropical insects). new features but on adaptations known from Typical desert species mitigate conditions by elsewhere that enable these small animals to specific behaviours such as body orientation and live in terrestrial habitats (Seely 1989). stilting, as well as by structural features. Al- Pools or streams that dry out seasonally or though some darkly coloured species bask when intermittently provide especially harsh condi- it is cool but avoid or orient away from direct sunshine when it is hot, and others limit heating tions to their typical occupants, which are through pale colours (Hamilton 1975), it has also adapted to aquatic habitats (sample reviews by been claimed that the primary roles of colour in Williams 1996, 1997). As water is removed, the desert animals are not thermal but for warning or habitats warm up, the concentration of ions camouflage (Cloudsley-Thompson 1979). increases, and the oxygen content decreases. Different kinds of temporary habitats vary espe- Despite a range of adaptive behaviours, most cially in the duration and season of drying and desert species must nevertheless resist extremes e.g. of heat and dryness by physiological means ex- in features of the surrounding terrain ( , cept during favourable periods. A few species Wiggins et al. 1980). The relatively small scale are resistant to temperatures up to 50 °C (Hadley of these interactions allows many species to 1975). Water is conserved by impermeable cuti- move to nearby permanent bodies of water dur- cles, especially additional lipid layers (Edney ing the dry period. Indeed, larger species fly ac- 1977), but some species can also tolerate consid- tively and may even overwinter in permanent erable losses of water (Zachariassen 1996) that ponds, exploiting temporary ponds only during would prove lethal to most temperate species the active season. Very small species such as (for other adaptations to dryness see also above). mites tend to use dispersing insect hosts or ver- In particular, although many species restrict wa- tebrate vectors to reach alternative habitats. ter loss through the cuticle, desert tenebrionid Several species withstand drought in situ by beetles also markedly reduce respiratory loss means of more or less impermeable coverings, through the spiracles by lowering metabolism. burying into the substrate, specialized cocoons This adaptation reduces cellular gradients of so- (e.g., Grodhaus 1980), and physiological adap- dium and hence amino acids, but the very high tations including anhydrobiosis. They may sur- efficiency of rectal reabsorption in these insects vive in the dried habitat all year or only part of allows the resulting extracellular amino acids to it (Wiggins et al. 1980). Specialized behaviours be recovered rather than excreted (Zachariassen are involved in the choice of habitats for sur- 1996). Cyclical respiration (see adaptations to vival in situ as well as movement to suitable dryness above) seems likely to be significant, es- waters elsewhere. As in other extreme habitats, pecially in dry habits such as deserts where most life cycles may be rapid or slow. Many species species have been able to reduce losses through inhabiting temporary ponds complete their life the cuticle itself to very low levels. The life cycles before the habitat dries, but others have

© 2007 Entomological Society of Canada 22 Can. Entomol. Vol. 139, 2007 prolonged development and survive the dry sea- and integration of many external and internal son in dormancy. elements. These components are summarized in A number of other widely distributed habitats Table 7. The ways in which development is are extreme in one or more respects, although modified, notably by changes in developmental there is less detailed information about the spe- rate or by interruption of development, form the cific adaptations of their insects. For example, basis of the responses. Environmental cues such bogs are characterized by extreme acidity, lim- as photoperiod and how and when they are re- ited nutrients, cool conditions, low oxygen, and ceived and integrated allow the developmental high water tables, and a limited but significant modifications to be controlled in relation to sea- fraction of the fauna is confined to or more sonal information. Overall patterns of develop- abundant in these habitats (Spitzer and Danks ment are structured through the number and 2006). Specialists even live inside the pitchers duration of delays and how they are integrated of insectivorous plants (e.g., Giberson and into one or more alternative life-cycle programs. Hardwick 1999). Such programs may include the movement of Salt marshes and seashores experience high insects from one habitat to another. Examining salinity and inundation by tides, and (in addi- patterns of variation helps in the interpretation tion to diet changes) species that live there tend of many of the responses. to have enhanced tolerance of salt (e.g., Giberson et al. 2001) or tolerance of submer- Developmental modifications gence by seawater (e.g., Sei 2004), and their Development can be modified (Table 7) by a activity is synchronized with the tides (Foster change in rate or by interruption. Quiescence 2000). Just as in the Arctic, mosquito eggs are interrupts development in direct response to positioned precisely in the oviposition habitat. ambient conditions that are not suitable (e.g., The salt marsh species Aedes sollicitans too cold for development) and is used for sea- (Walker) places them high enough to exclude sonal control in some species (e.g., Dendrocto- daily flooding but in range of the higher lunar nus: Powell and Jenkins 2000; Powell and tides that occur every 2 weeks (Knight and Logan 2005). However, most species interrupt Baker 1962; Crans 2004). In areas subject to development in a programmed diapause stage, wave action, the availability of sheltered which typically anticipates unfavourable condi- microhabitats is especially important (Pugh and tions and is insensitive to otherwise favourable Mercer 2001). Again, therefore, adaptations in conditions until after a delay. Moreover, the du- coastal insects are both ecological, such as hab- ration of this delay varies (diapause intensity; itat choice and timing, and physiological, such see below). Although such interruptions in de- as osmoregulation. velopment have attracted the most attention, Information from these different extreme programmed adjustment of the duration of de- habitats confirms several generalizations about velopment by slowed or accelerated growth is insect adaptations. Species can cope with ex- also extremely common in insects. treme conditions only by multiple simultaneous Developmental modifications are governed in adaptations of ecology and physiology. There is different ways in different species; they include no single “required” adaptation, but three main both fixed genetic and environmentally con- kinds of responses help to solve the problems trolled plastic responses and range from a sin- posed by difficult conditions: movement, as gle one-time response to the continuous among ponds or into sheltered or otherwise fa- adjustment of developmental rates throughout vourable habitats; resistance, such as cold har- at least the larval stages (Danks 1994). Most diness and drought tolerance; and life-cycle or species continue to develop unless delays are behavioural adaptations, including circadian induced by specific signals (Danks 2002b). rhythms or opportunistic behaviour, dormancies, There are many typical instances of this sort and rapid or prolonged development. Conse- whereby winter diapause is induced by short quently, different suites of multiple adaptations photoperiods. Such an “active” default allows are found in different species. development at any time unless a reliable signal of impending unsuitability is received. On the Control and integration other hand, in many species from habitats that are intermittently unfavourable or in which envi- The timing of insect life cycles in relation to ronmental signals do not reliably predict future the seasons is controlled through the assembly unsuitability, “passive” responses are more

Table 7. Control elements and integration.

Element Components or alternatives Developmental modifications Type of modification Developmental rate, quiescence, or diapause Type of response Single or continuous, fixed or plastic Default developmental response Active development or passive delay Default response after delay Standard rate or accelerated rate Variability Little variation, normally distributed vs. wide or discontinuous variation, programmed Sensitivity to environmental signals Type of sensitivity Insensitive, intermittently sensitive to continuously responsive Effective cues None to many; cues include photoperiod, temperature, food, moisture, and others Type of sensitivity Qualitative or quantitative, fixed or changing through stage Sensitive stage One to many stages; various relationships to responsive stage Life-cycle patterns Type of life-cycle control Direct or indirect control, single or multiple factors and influences Number of dormancies One, multiple, or successive Number of components in a single One, few, or many dormancy Duration of dormancy Short, long or very long, fixed or variable Number of successive diapause inductions One or more possible in same stage Duration of life cycle, voltinism Days to years, <1 to many generations/year Number of alternative life-cycle routes None to many (fixed or simple life cycle vs. complex life cycle with multiple pathways) Time budgeting Time gained, conserved, monitored, or wasted common. In these instances delay is the default results have led to the erroneous belief that the option, and active development has to be in- delays termed “obligate diapause” are inevita- duced by environmental suitability or reliable ble and qualitatively different from other envi- temporal signals (Danks 2002b, 2006a). For ex- ronmental responses. In fact, these “obligate” ample, a number of short days followed by a responses are rare. number of long days — a completely unambigu- ous signal that summer is coming — are needed Sensitivity to environmental signals for reproductive development to occur in some Environmental signals are used in many ways carabid beetles and other insects (Thiele 1975; to control seasonal development (Table 7). Rel- review by Danks 1987a, Table 23). Comparable atively few species are insensitive to environ- alternatives occur in the completion of mental information, and even some of those diapause. Many species resume development as believed to be insensitive to photoperiod, for inhibition diminishes with time at a standard example, prove to be sensitive only to particular rate (“horotelic”), but in other species the inhi- changes that are not always included in labora- bition can be removed faster as a result of ex- tory protocols (see passive responses in the pre- ternal signals (“tachytelic”) (Hodek 1981, 1983; ceding section). Many species are sensitive at Košt’ál et al. 2000). only one stage or for only a limited part of one Passive responses, in which development re- stage. In other species, more stages are sensi- quires particular sequences of environmental tive (see below). A few species integrate envi- conditions, give rise to individuals that fail to ronmental information continuously throughout develop during simple experiments. Such the life cycle and adjust development

© 2007 Entomological Society of Canada 24 Can. Entomol. Vol. 139, 2007 accordingly. For example, complex ongoing re- Moreover, in many species the response to a actions of growth rate and diapause in response particular signal changes through development, to photoperiod and temperature program the life even within the same stage. Commonly, this recycle in the dragonfly Aeshna viridis Eversman sults from differences in sensitivity (see below) (Aeshnidae) (Norling 1971; Danks 1991a). but in addition the response itself can change. Although photoperiod is the best known cue, For example, long photoperiods that stimulate different species use different environmental rapid growth in young larvae slow growth in information. Photoperiod, light intensity, tem- older ones (examples reviewed by Danks perature level, thermoperiod, food, moisture, 1991a). Even in a single species, responses can density, mating, and chemical cues have all be all-or-none as well as graded, the number of been reported to influence diapause induction in instars can vary, and responses can change one species or another (Danks 1987a, 1994, Ta- through development (Tanaka et al. 1999). ble 2), and even the presence of predators may Diapause development in insects typically re- have an effect (Kroon et al. 2005). Many of duces the sensitivity to photoperiod or reduces these cues, especially temperature, also influ- the critical photoperiod (discussion by Danks ence the progress of diapause (diapause devel- 1987a, pp. 154–155). opment). And, although it has been less studied, Finally, the effective use of environmental growth rate is controlled not only by the direct signals depends on the stage or stages of sensi- action of temperature level and density or food tivity and how close they are to the stage that limitation, but also by many factors that act as responds. Despite great variations among spe- cues, including photoperiod and density (Danks cies and exceptions to normal tendencies, sev- 1987a, Tables 33, 36) as well as light intensity, eral generalizations can be made about this temperature, food, moisture, and chemical sig- sensitivity (cf. Danks 1987a, pp. 80–81). First, nals (Danks 1987a, 1994). Moreover, these en- sensitivity tends to be greater in active stages vironmental elements typically interact and exposed to the environment and with better de- responses to more than one of them are inte- veloped sense organs, and hence larvae and grated. The best known interaction is that be- adults are more often or more markedly sensi- tween photoperiod and temperature (Danks tive than eggs or pupae. Second, most often the 1987a; Saunders 2002). sensitive stage only just precedes the stage that Life style and habitat determine which cues responds, a timing that is not surprising because are most informative for a given species. For cues as to future conditions typically are most example, production of dispersing or dormant reliable closer to the time for which prediction stages depends on food or density in environ- is needed. Third, many species add (not substi- ments where the conditions of the food can de- tute) sensitivity in earlier stages as well, thereby teriorate rapidly, as for some aphids and mites monitoring conditions over a longer period, (e.g., De Barro 1992; Corente and Knülle 2003). which might compensate for variation and al- Species also differ in how the signals are per- low ambiguous signals to be resolved. In such ceived or summed. Many species respond to instances sensitivity typically increases towards whether photoperiods are above or below a criti- the end of the sensitive stage so that more cal length, but the length of the photoperiod has weight is given to the most recent experience, no influence other than its position above or be- but alternative information received earlier is low that critical length. However, an increasing available if current signals are neutral or ambig- number of species have been reported to show uous. Theoretically, the tendency to use recent quantitative responses, whereby the degree of cues would be offset by the fact that early de- response accords with the actual duration of termination gives more time for the food stor- the photoperiod or the level of the temperature. age and other metabolic adjustments required to This phenomenon was even held to be typical survive diapause. This requirement, and the rather than exceptional by Zaslavski (1988, need to integrate cues over a finite interval 1996). Quantitative responses have been reliably (e.g., a certain minimum number of short day- reported for the rate of growth (Suzuki and lengths), extends the duration of the sensitive Tanaka 2000), the incidence of diapause period in many species, even though it ends just (Kimura 1990), the intensity of subsequent before the developmental decision it governs. diapause (Nakamura and Numata 2000; Nevertheless, these generalizations are by Kalushkov et al. 2001), and the intensity during no means universal. Larvae of the moth Cydia diapause (Nakamura and Numata 2000). pomonella (Linn.) (Tortricidae), which feed

© 2007 Entomological Society of Canada Danks 25 inside apples, have early, not late, sensitivity larvae grow more slowly (e.g., Danks 1987a, (e.g., Jermy 1967; Peterson and Hamner 1968), Table 34; McGregor 1997), females that have presumably because photoperiodic cues are experienced diapause during development are masked inside the food source later in life. The less fecund (e.g., Ishihara and Shimada 1995; sensitive and responsive stages are widely sepa- Bradshaw et al. 1998; review by Danks 1987a), rated in a few spectacular examples, of which and fast or slow later growth can compensate the best known is the sensitivity of eggs of the for slow or fast early growth (Volney and silk worm Bombyx mori Linn. (Bombycidae) Liebhold 1985). for egg diapause in the next generation (Kogure Dormancy lasts for a short or long fixed time 1933; many subsequent papers). in some species, but in most species its induc- The fact that multiple cues are integrated in tion and end depend on environmental condi- different ways in different species means that tions. Extended periods of diapause have experimental designs that are too simple may attracted the most attention (see below), but ac- cause relevant factors to be undervalued. Ancil- tually there are many ways of extending devel- lary cues are easy to overlook if there is an un- opment in addition to a long single diapause, due preoccupation with photoperiods. Often the including slow development, dispersed repro- stage(s) of response cannot be determined accu- ductive effort, and repeated diapause, as shown rately without multiple, rather than the usual for several species of beetles (Topp 2003). simple, experimental switches from one regime Some species even undergo repeated interrup- to another during development. tions of development in the same stage, as exemplified by multiple quiescences and dia- Life-cycle patterns pauses in eggs of some grasshoppers Life cycles are patterned (Table 7) by the (Wardhaugh 1980; Ingrisch 1986). Successive timing and duration of substages. In some spe- reinductions of diapause are known in adults of cies the substages are controlled relatively sim- several Heteroptera (Hodek 1971; references in ply, for example by the direct effects of Danks 2002a). Other species have diapause as temperature, but in most species in seasonal en- successive control points in the life cycle at sev- vironments more complex control is exerted by eral different stages (Danks 1991a; Tanaka and multiple token stimuli such as photoperiod. Zhu 2004). Species also differ in how many dormancies Given these many possible ways to introduce intervene in the life cycle. Dormancy in the delay into the life cycle, some very long life cy- broadest sense can include adjustments of cles are known in which one completed genera- growth rate (see above) as well as diapause and tion can last for many years. Very long life quiescence (Danks 1987a). Typical species cycles are associated in particular with poor- have a single diapause during the adverse sea- quality food and cold environments, but also son, but many other patterns are known (Masaki with unpredictable circumstances (Danks 1992). 1980; Danks 1987a). In typical species, one or Moreover, many species adjust the life cycle more dormancies enforce a life cycle of exactly continually or at intervals in response to envi- one year. Some species have multiple diapauses ronmental cues, so that different alternative across several years (Nishizuka et al. 1998 for routes including very long durations are possi- Lepisma; Ingrisch 1986 for grasshopper eggs). ble in a single species (e.g., Danks 1991a). For Moreover, each dormant period may consist of example, egg development of the grasshopper several phases, each of them potentially under Chortoicetes terminifera (Walker) (Acrididae) environmental control. Thus diapause develop- has no fewer than 18 alternative routes, modi- ment consists of two or more stages (e.g., fied by the presence and duration of diapauses Nomura and Ishikawa 2000) and ovarian dia- and quiescences in several stages under the con- pause comprises multiple steps (e.g., Košt’ál trol of photoperiod, temperature, and moisture and Šimek 2000). Development then proceeds (Wardhaugh 1986; see Danks 1991a). Develop- very differently according to the pattern of con- ment of the mite Lepidoglyphus destructor ditions (Higaki and Ando 2005). Such stages (Shrank) (Glycyphagidae) reflects genetic and are linked, both because an earlier phase must environmental inputs that bypass the hypopal be completed before a later phase can begin and stage (resting deutonymph) or interpolate it for because the occurrence of one phase may mod- a period of a few days to many months (Knülle ify subsequent development. For example, in 1991a, 1991b; see Danks 1994). Other species some species (but not in all) diapause-destined use different pathways to integrate other

adaptations with the time of year that adults emerge. For example, the butterfly Pararge aegeria (Linn.) (Nymphalidae) couples larval diapause, pupal diapause, or direct development that results in emergence during different seasons with sex-related morphological differences associated with flight and thermoregulation (Van Dyck and Wiklund 2002). Species budget time to take account of seasonality, resource levels, and so on. When an extra generation is not feasible in any event even with spare time (because of seasonal resources or other constraints), some species simply waste the extra time through very slow growth or stationary moults, thereby maintain- ing appropriate seasonal synchrony (see also Trade-offs). At the other end of the spectrum, species may gain time by adaptations that in-

laboratory selection of generations; unpredictable annual resources clude developing rapidly in all stages, exploiting See below Selective pressure Long suitable season; laboratory stress Continuous change in growing season but unit change in no. rich food, eliminating stages, reducing resource investment by reducing size, fecundity, longevity, and structural complexity, accelerating development through such means as basking and rapid reproduction, and choosing the most suit-

specific able, especially the warmest, microhabitats.

vs. Multiple coincident adaptations of this sort allow extremely rapid development especially in species of very small size, giving generation times as short as 4 days (for detailed examples see Danks 2006c). evolved response slowly development prolonged diapause

Variance changes rapidly or Types of variation Patterns of variation provide important information about the control of seasonal responses especially in relation to environmental variation (see Table 8). Background patterns of variation reflect differences among individuals and can be characterized from normality, skew, and other typical statistics. Individual differences stem from small genetic variations among individuals as adaptive General variation well as from small differences in the conditions

vs. that each individual may experience even in the same habitat, in insects especially because of

pattern of variation differences from one microhabitat to the next or from one part of the microhabitat to another. From the perspective of seasonal adaptations, the most interesting differences are between variations that simply reflect this background of general individual variation and variations that

Summary of the types of variation involved in seasonal patterns. have evolved to provide advantages in particular environmental circumstances, as explained below. Finally, the rate at which patterns of Individual variationType of response Individual differencesChange in response Stochastic Temporal Amount spread and speed ofNarrow change in the BroadDiscontinuous Normality, skew Restricted Discrete modes Wide, continuous Genetic and environmental variation Synchronous emergence Prolonged Split emergence; cohorts; staggered sawtooth clines; Restrictive temperature threshold; multiple thresholds; Basic elements Coincident variation Temporal and other changes are integrated Seasonal change in quality Resources change through the season Table 8. Type of variation Description of variation Sample responsesvariation Sample correlates respond to selective forces gives

© 2007 Entomological Society of Canada Danks 27 additional insights into how environments af- laboratory experiments, however, because inade- fect the evolution of the patterns. quate conditions cause unnatural delays and in- The roles of individual variation in evolved crease variation in the duration of development. responses can be reviewed by recognizing three These limitations stem not only from the quan- overall patterns of variation: narrow, broad but tity or quality of food for larvae, but also from continuous, and discontinuous (compare Fig. 1). temperatures, light intensity, ancillary food, and Variations restricted to a short time period, a so on that are required for normal reproductive small size range, and so on normally accord activity (e.g., Danks 2000c). with predictable environments that may be suit- Discontinuous patterns of variation such as able for a relatively short period (for the current bimodal emergence, cohort splitting, and dia- or next generation), although synchrony has pause by a fraction of the population for more other advantages such as coincidence of indi- than one year are especially instructive for un- viduals for reproductive activity. Narrow varia- derstanding seasonal responses. A few of these tions often are under environmental or seasonal patterns reflect short-term environmental con- control, such as a single temperature threshold. trol, such as two pulses of emergence in warm The diapause of many species serves to accu- weather separated by a lull during a cold spell mulate individuals in exactly the same stage by (cf. Fig. 1D above). However, most broad and the end of winter; emergence is thus delayed discontinuous patterns of variation appear to re- until spring and brought under the direct control flect ways to overcome the unpredictability of of heat accumulations. In turn, emergence in natural environments (Danks 1983, 1987a, spring of several species requires a relatively chap. 9). Such bet-hedging or risk-spreading re- high temperature that synchronizes the appear- sponses occur in a wide range of taxa and envi- ance of adults. ronments. For example, pupal development in In some species multiple thresholds and dif- the moth Epirrita autumnata (Borkhausen) ferences among stages enhance synchrony. For (Geometridae) lasts from 1 to 3 months, a vari- example, in some dragonflies young larvae de- ance that would be adaptive in spreading the velop at a lower temperature than older larvae risk of mortality from low temperatures and and so catch up during spring (Lutz 1968, 1974). In chironomid midges temperature thresholds predation (Tammaru et al. 1999). Eggs of the increase successively through larval activity, bush cricket Ephippiger ephippiger (Fiebig) growth, pupation, and emergence (Danks and (Tettigoniidae) hatch over a very long interval Oliver 1972a). Other species use photoperiod as a result of maternal influences, including too to synchronize development, as in some of maternal age, on diapause; this variation has the life-cycle pathways already noted. In addi- been interpreted as providing insurance against tion, but with less explanatory relevance, lab- the low predictability of future environmental oratory experiments sometimes enhance conditions (Hockham et al. 2001). Larvae of synchrony because only individuals with a cer- the burnet moth Zygaena trifolii (Esper) tain pattern of development are favoured by the (Zygaenidae) vary widely in the duration of culture conditions. Such biases may select for a pre-diapause development and consequently in laboratory strain with an unduly narrow range the instar in which diapause occurs, and the of variation (Miyatake and Yamagishi 1999; variation is genetically based (Wipking and Danks 2000c). Kurtz 2000). It appears to reflect the temporal Broad but continuous patterns of variation can and spatial unpredictability of the habitats of exploit wider spatial, temporal, or nutritive re- this species. Glycyphagus mites produce di- sources. Species of several taxa are characterized rectly developing, dormant phoretic, and dor- by wide variations in development (e.g., Aquino mant sedentary forms under complex genetic and Turk 1997; Stiefel et al. 1997). Very long and environmental control (Knülle 2003): ge- emergence and subsequent oviposition into habi- netic variation spreads risk, and current re- tats that remain suitable all summer is character- sponse to food levels adjusts the proportions of istic of many aquatic insects in temperate and the different forms. The blue butterfly Scoli- tropical habitats (“summer species” of Corbet tantides orion (Pallas) (Lycaenidae) accumu- 1964a). When development is staggered (from lates diapause pupae from each summer the long duration of oviposition or through de- generation, not just from the final one, maxi- velopmental variation), resources are less likely mizing the number of generations whilst insur- to be overloaded. Caution is required in ing against failures (Trankner and Nuss 2005).

Egg hatch varies widely and erratically in adaptive over very long time frames (necessitat- stoneflies from unpredictably wet streams in ing a way to “protect” the variation), its proper Australia (Hynes and Hynes 1975). For exam- analysis in the context of unpredictable envi- ple, eggs of Dinotoperla serricauda Kimmins ronments will be very difficult. Analysis of pro- (Gripopterygidae) began to hatch only after longed diapause in parasitoids of hosts that more than 30 weeks following their collection enter prolonged diapause (Koziol 1998; Corley and continued to hatch for 70 more weeks. Ex- and Capurro 2000; other examples in Danks tended hatch is characteristic of temperate 1987a, Table 27) would also be informative. Isogenoides species (Sandberg and Stewart Multiple features of seasonal responses can 2004). Wide genetic variations in the date of be integrated through patterns of variation. For egg hatch in the moth Malacosoma americanum example, resources that change through the sea- (Fabr.) (Lasiocampidae) (independent of tem- son can be exploited by programmed changes perature) appear to offset the risk of loss of in individual quality. These changes are medi- young larvae due to storms in late winter (Neal ated by the age of the mother in a number of et al. 1997). species (review by Mousseau and Dingle 1991), The desert bee Perdita portalis Timberlake but the effects on fitness of such complex inter- (Andrenidae) commits only about half the pu- actions are very difficult to quantify and inter- pae to development even under optimal condi- pret (and see Trade-offs). For example, young tions; also, individuals of low body weight are larvae of the grasshopper Chorthippus brunneus more likely to emerge, and emergence occurs (Thunberg) (Acrididae) find better conditions directly in response to high humidity (Danforth early in the season, but the later eggs and hence 1999). Some attempts have been made at theo- hatchlings are larger (Cherrill 2002). Maternal retical analysis of strategies for delayed devel- fitness in this species is greater with many opment (e.g., Bradford and Roff 1997), so far small eggs when conditions are good but with limited resolution for the examples of greater with few large eggs when conditions are most interest that include genetically deter- poor, near the edge of the range (Hassall et al. mined polymorphisms (contrast Hopper 1999, 2006). who excluded such examples). In summary, the extent of individual variation In many species, some individuals enter dia- differs widely among species and for different pause for more than one adverse season (Danks aspects of the response. In particular, some 1987a, Table 40), with decreasing proportions characteristics have narrow, normally distrib- of the population remaining in diapause through uted variations that synchronize populations successive years. In extreme cases these pro- with favourable environments, while others show longed diapauses can last for 30 years or more wide or multimodal variations adaptive espe- (Powell 2001 for yucca moths). Typical species cially to environmental unpredictability. All of come from habitats that are unpredictable, such these patterns of variation reinforce the conclu- as the Arctic, deserts, plants with intermittent sion that seasonal adaptations reflect the nature fruiting, and so on, but prolonged diapause also of environments and the ways that they vary on occurs at low levels in many species from more a range of scales. ordinary environments. Geographical as opposed to individual pat- Prolonged diapause appears to have a com- terns of variation also provide insights into en- plex genetic basis (Danks 2006a). Therefore, vironmental pressures. Very common are clines although it ends in some species in response to of response, with gradual changes in size or environmental cues (e.g., Masaki 2002; Higaki other features with latitude. Increase in size 2006), the onset appears to be genetically pro- with latitude appears to be driven by tempera- grammed in most species, either by genetic ture, because insects developing more slowly at polymorphism comprising different genotypes lower temperatures are often larger (but see in long-term balance or by stochastic poly- Walters and Hassall 2006); however, decrease phenism (Walker 1986) generating variability in size with latitude accords with season length, from a single genotype (also termed coin- as shorter seasons limit further growth (review flipping plasticity or diversified bet hedging: by Blanckenhorn and Demont 2004). The clines Menu and Debouzie 1993; Menu and Desouhant can also be modified by factors such as food 2002; Menu et al. 2000). Because prolonged availability (Chown and Klok 2003b). diapause affects only a small proportion of the These clinal patterns depend on voltinism, population in most species and typically is because multivoltine species are not constrained

(except near the end of the season) in the same Coupled with the challenging complexity of way as univoltine ones (Blanckenhorn and seasonal adaptations is the fact that usually the Demont 2004). Bivoltine populations may de- same selective forces from the environment can velop faster than univoltine ones to achieve the be overcome in many different ways. For exam- second generation (Burke et al. 2005). In par- ple, temporary adversity can be met through ticular, resources such as growing season diapause, changed developmental rate, resis- change gradually across space, whereas a sea- tance, or other means. Hence, it is not possible sonal response may be possible only in the dis- to tabulate any simple set of “seasonal re- crete units of a generation. Hence, for example, sponses”. Despite the complexity, seasonal ad- the size of individuals may decline with grow- aptations nevertheless fall into recognizable ing season up to the point that a generation is geographical and temporal patterns such as the lost because the season is now too short to various clinal responses, life-cycle sequences, complete the extra generation successfully. Size and sets of adaptations to adversity already then increases dramatically before its slow de- summarized in preceding tables. Such summa- cline resumes. Such sawtooth geographic clines ries confirm that it is feasible to analyze the have been shown in many orthopteroids and patterns at very broad as well as narrow scales. also in butterflies, beetles, and other taxa (e.g., Likewise, it is necessary to examine relatively Masaki 1978; Roff 1980; Nylin and Svärd complex systems and simultaneous trade-offs. 1991; Ishihara 1998). Life cycles can be patterned by many successive or simultaneous developmental options Conclusions (see Life-cycle patterns above). The effects of responses to the environment may ripple Understanding seasonal adaptations requires through several generations (Mondor et al. a broad view of the effects of temporal, spatial, 2005 for the effects of predation). and resource patterns. Although it is easier to This review confirms that the key to under- work with only part of this huge conceptual ter- standing all of the adaptations lies in the spe- ritory, as most scientists have done, real organ- cific nature of the environment (cf. Table 1). isms integrate a great array of factors The seasonal responses of movement, habitat simultaneously. Such a framework leads to selection, habitat modification, and resistance to great complexity of selective pressures and re- cold, dryness, and food limitation all stem from sponses. Consequently, even a single trait can environmental pressures. Limitation of environ- relate to multiple seasonal functions. For exam- mental resources forces the wide variety and ple, as pointed out by Danks (2002a), slow de- great complexity of trade-offs. Environments velopment can help to conserve energy, protect are implicated in the patterns of variation. Espe- against adversity, synchronize individuals with cially striking is the contrast between equable one another or with food, optimize the timing habitats with reliable signals and varying and of reproduction, prevent development at risky unpredictable ones inhabited by species show- times of year, and monitor environments for ing a variety of patterns of variation that serve longer periods to allow more reliable develop- as bet-hedging strategies. mental decisions. All of these roles have been Detailed knowledge about environments is demonstrated in various species, and slow de- therefore required. This point has been made velopment typically serves more than one role for many years about cold-hardiness studies, for simultaneously. The opposite trait, extremely example (e.g., Danks 1978, 1996, 2006a). Even rapid development, can help to accelerate popu- so, most studies of cold hardiness still focus lation growth, exploit ephemeral or limited re- only on physiological and biochemical adapta- sources, and escape natural enemies or tions without the detailed information about the approaching climatic adversity and can serve conditions experienced and their patterns of other roles in special cases (for example, where natural variation that would help to explain the males are parasitic on their own females). In nature and incidence of the physiological and particular, and reinforcing the complexity just biochemical adaptations. Most studies of life- noted, abbreviated life cycles have been cycle adaptations likewise lack parallel environ- achieved in many ways, including small size, mental data. In contrast, knowledge of spring rapid development, elimination or reduction of weather patterns, for example, has allowed the stages, and microhabitat choice (see Life-cycle variability of spring hatch or emergence to be patterns above). interpreted as a means of insuring against harsh

© 2007 Entomological Society of Canada 30 Can. Entomol. Vol. 139, 2007 interludes early in the season (e.g., Bradshaw Bale, J.S., Worland, M.R., and Block, W. 2001. Ef- 1973; Neal et al. 1997). By the same token, we fects of summer frost exposures on the cold toler- can understand how seasonal adaptations such ance strategy of a sub-Antarctic beetle. Journal of as prolonged diapause are maintained and gov- Insect Physiology, 47: 1161–1167. erned in a given species only through the long- Baust, J.G., and Nishino, M. 1991. Freezing toler- Eurosta term analysis of habitat variability for that spe- ance in the goldenrod gall fly ( solidaginis). In Insects at low temperature. Edited cies. by R.E. Lee, Jr. and D.L. Denlinger. Chapman and These observations reinforce the value of wider Hall, New York. pp. 260–275. approaches than have been customary. I con- Bayley, M., and Holmstrup, M. 1999. 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