Entomology 3rd edition - C.Gillott - Chapter 22 pdf

This relationship will hold even when thetemperature fluctuates, provided that the fluctuations do not exceed the range of linearity.The temperature limits outside which development ceases

Ecology

an immediate effect on the orientation of an insect as it searches for food, and may inducechanges in an insect’s physiology in anticipation of adverse conditions some months in thefuture Another abiotic factor to which insects are now routinely subjected (deliberately orotherwise) are pesticides Apart from the obvious effect of lethal doses of such chemicals,pesticides may have more subtle, indirect effects on the distribution and abundance ofspecies, for example, alteration of predator-prey ratios and, in sublethal doses, changes infecundity or rates of development.

Under natural conditions organisms are subject to a combination of environmentalfactors, both biotic and abiotic, and it is this combination that ultimately determines thedistribution and abundance of a species Frequently, the effect of one factor modifies thenormal response of an organism to another factor For example, light, by inducing diapause(Section 3.2.3), may make an insect unresponsive to (unaffected by) temperature fluctua-tions As a result, an insect is not harmed by abnormally low temperatures, but nor does

it become active in temporary periods of warmer weather that may occur in the middle ofwinter

2 Temperature

2.1 Effect on Development Rate

The body temperature of insects, as poikilothermic animals, normally follows closelythe temperature of the surroundings Within limits, therefore, metabolic rate is proportional

to ambient temperature Consequently, the rate of development is inversely proportional

to temperature (Figure 22.1) Outside these temperature limits the rate of development

no longer bears an inversely linear relationship to temperature, because of the deleteriouseffects of extreme temperatures on the enzymes that regulate metabolism, and eventuallytemperatures are reached (the so-called upper and lower lethal limits) where death occurs

655

CHAPTER 22

FIGURE 22.1. Relationship between temperature and rate of development in eggs of Drosophila melanogaster

(Diptera) The two curves represent different ways of expressing this relationship, each being the reciprocal of the

other [After H G Andrewartha, 1961, Introduction to the Study of Animal Populations, University of Chicago

Press By permission of the author.]

Within the range of linearity the product of temperature multiplied by time required fordevelopment will be constant This constant, known as the thermal constant or heat budget,

is commonly measured in units of degree-days This relationship will hold even when thetemperature fluctuates, provided that the fluctuations do not exceed the range of linearity.The temperature limits outside which development ceases and the rate of development at

a given temperature vary among species, two seemingly obvious points that were apparentlyoverlooked in some early attempts at biological control of insect pests A predator that, onthe basis of laboratory tests and short-term field trials, had good control potential was found

to exert little or no control of the pest under natural conditions Further study showed this

to be related to the differing effects of temperature on development, hatching, and activitybetween the pest and its predator

A broad correlation exists between the temperature limits for development and thehabitat occupied by members of a species For example, many Arctic insects that overwinter

in the egg stage complete their entire development (embryonic+ postembryonic) in thetemperature range 0◦C to 4◦C, whereas in the Australian plague grasshopper, Austroicetes cruciata, development ceases below 16◦C This means that the distribution of a species will

be limited by the range of temperature experienced in different geographic regions, as well

as by other factors However, the distribution of a species may be significantly greater thanthat anticipated on the basis of temperature data for the following reasons: (1) temperatureadaptation may occur, that is, genetically different strains may evolve, each capable ofsurviving within a different temperature range; (2) the temperature limits of developmentmay differ among developmental stages [this also serves as an important developmentalsynchronizer in some species (Section 2.3)]; and (3) the insect may have mechanisms forsurviving extreme temperatures (Section 2.4)

657 THE ABIOTIC ENVIRONMENT

Because of the ameliorating effects of the water surrounding them, aquatic insects

are not normally exposed to the temperature extremes experienced by terrestrial species

Further, because ice is a good insulator, development may continue through the winter in

some aquatic species in temperate climates, though air temperatures render development

of terrestrial species impossible Indeed, through evolution there has been a trend in some

insects (e.g., species of Ephemeroptera and Plecoptera) to restrict their period of growth

to the winter, passing the summer as eggs in diapause Such species, whose developmental

threshold is usually only slightly above 0◦C, appear to gain at least two advantages from

this arrangement First, through the winter there is an abundance of food in the form of

rotting vegetation, yet relatively little competition for it Second, they are relatively safe

from predators (fish) which are sluggish and feed only occasionally at these temperatures

(Hynes, 1970b) Such a life cycle may also allow some species to inhabit temporary or still

bodies of water that dry up or become anaerobic during summer

2.2 Effect on Activity and Dispersal

Through its effect on metabolic rate, temperature clearly will affect the activity of

insects Many of the generalizations made above with regard to the influence of temperature

on development have their parallel in relation to activity Thus, there is a range of temperature

within which activity is normal, though this range may vary among different strains of the

same species The temperature range for activity is correlated with a species’ habitat; for

example, in the Arctic, chironomid larvae are normally active in water at 0◦C, and adults

can fly at temperatures as low as 3.5◦C (Downes, 1964)

By affecting an insect’s ability to fly temperature may have a marked effect on a species’

dispersal and, therefore, its distribution Further, because flight is of such importance in food

and/or mate location and, ultimately, reproduction, temperature is of great consequence in

determining the abundance of species Insects use various means of raising their body

temperature to that at which flight is possible even when the ambient temperature is low

For example, they may be darkly colored so as to absorb solar radiation, or they may bask

on dark surfaces, again using the sun’s heat Some moths and bumblebees beat their wings

while at rest and simultaneously reduce hemolymph circulation in order to increase the

temperature of the thorax (Chapter 17, Section 3.1) A dense coat of hairs or scales covers

the body of some insects, which, by its insulating effect, will retard loss of heat generated

or absorbed

In extremely cold climates these physiological, behavioral, or structural features may

no longer be sufficient to enable flight to occur, especially in a larger-bodied, egg-carrying

female Thus, different temperature-adaptation strategies are employed, some of which

are exemplified especially well by Arctic black flies (Simuliidae: Diptera) Typical adult

temperate-climate species are active insects that mate in flight, and females mayfly

consid-erable distances in search of a blood meal necessary for egg maturation In contrast, females

of Arctic species seldom fly Their mouthparts are reduced and eggs mature from nutrients

acquired during larval life Mating occurs on the ground as a result of chance encounters

close to the site of adult emergence In two species parthenogenesis has evolved, thereby

overcoming the difficulty of being found by a male (Downes, 1964)

Temperature change, through its effect on the solubility of oxygen in water, may

markedly modify the activity and, ultimately, the distribution and survival of aquatic

in-sects Members of many aquatic species are restricted to habitats whose oxygen content

remains relatively high throughout the year Such habitats include rivers and streams that are

CHAPTER 22

normally well oxygenated because of their turbulent flow and lower summer temperature,and high-altitude or -latitude ponds and lakes, which generally remain cool through thesummer Alternatively, as noted in Section 2.1, the life cycle of some species is such thatthe warmer (oxygen-deficient) conditions are spent in a resistant, diapausing, egg stage

2.3 Temperature-Synchronized Development and Emergence

Many species of insects have highly synchronized larval development (all larvae aremore or less at the same developmental stage) and/or synchronized eclosion, especially thosethat live in habitats where the climate is suitable for growth and reproduction for a limitedperiod each year Synchronized eclosion increases the chances of finding a mate It may alsoincrease the probability of finding suitable food or oviposition sites, or of escaping potentialpredators Synchronized larval development also may be related to the availability of food,and in some situations it may be necessary in order to avoid interspecific competition for thesame resource For certain carnivorous species, such as Odonata, synchronized developmentmay help reduce the incidence of cannibalism among larvae

Perhaps not surprisingly in view of its effects on rate of development and activity,temperature is an important synchronizing factor in the life of insects Its importance may

be illustrated by reference to the life history of Coenagrion angulatum, which, along with

several other species of damselflies (Odonata: Zygoptera), is found in or around shallowponds on the Canadian prairies (Sawchyn and Gillott, 1975) For these insects the seasonfor growth and reproduction lasts from about mid-May to mid-October For the remaining 7

months of the year C angulatum exists as more or less mature larvae, which, between about

November and April, are encased in ice as the ponds freeze to the bottom (The larvae selves do not freeze, as the ice temperature seldom falls more than a few degrees Celsius

them-below zero as a result of snow cover.) In C angulatum both larval development and eclosion

are synchronized by temperature Synchronized development is achieved (1) by means ofdifferent temperature thresholds for development in different instars, that is, younger larvaecan continue to grow in the fall after the growth of older larvae has been arrested by decreas-ing water temperatures, and (2) by a photoperiodically induced diapause Thus, samplescollected in mid-September include larvae of the last seven instars, whereas those from earlyOctober are composed almost entirely of larvae of the last three instars Conversely, after theice melts the following April, younger larvae can continue their development earlier thantheir more mature relatives, so that by mid-May more than 90% of the larvae are in the finalinstar After their release from the ice larvae migrate into shallow water at the pond marginwhose temperature parallels that of the air Emergence occurs when the air temperature is

20◦C to 21◦C (and the water temperature is about 12◦C) It begins normally during the last

week of May and reaches a peak within 10 days Emergence of C angulatum follows that

of various chironomids and chaoborids (Diptera), which form the main food of the adultdamselflies during the period of sexual maturation The development and emergence ofother damselfly species that inhabit the same pond are also highly synchronized but occur

at different times of the growing season This enables the species to occupy the same pondand make use of the same resources, yet avoid interspecific competition This is discussedfurther in Chapter 23 (Section 3.2.1)

Though unpredictable on a day-to-day basis, temperature does have a regular seasonalpattern that controls the onset and termination of diapause in some species Temperature isthe primary diapause-inducing stimulus for some subterranean species [e.g., some groundbeetles (Carabidae)], wood- and bark-inhabiting species, and pests of stored products that

659 THE ABIOTIC ENVIRONMENT

live in darkness It also is the major cue for diapause induction in some insects living

near the equator where changes in photoperiod are too small to act as signals of seasonal

change (Tauber et al., 1986; Denlinger, 1986) Temperature can also exert a strong

influ-ence on diapause and other photoperiodically controlled phenomena, as is discussed below

(Section 3.2)

2.4 Survival at Extreme Temperatures

In many tropical areas climatic conditions are suitable for year-round development and

reproduction in insects In other areas of the world, the year is divisible into distinct seasons,

in some of which growth and/or reproduction is not possible One reason for this arrest of

growth and/or reproduction may be the extreme temperatures that occur at this time and are

potentially lethal to an insect In many instances shortage of food would also occur under

these conditions

To avoid the detrimental effects of periods of moderately low (down to freezing) or high

temperature, and to ensure that development and reproduction occur at favorable times of the

year, insects use an array of behavioral and physiological mechanisms (Danks, 2001, 2002)

First, the life history of many species is arranged so that the period of adverse temperature

is passed as the immobile, non-feeding egg or pupa Second, prior to the advent of adverse

conditions [and it should be realized that the token stimulus that triggers this behavior is not,

in itself, adverse (see Section 3.2)], an insect may actively seek out a habitat in which the

full effect of the detrimental temperature is not felt For example, it may burrow or oviposit

in soil, litter, or plant tissue, which acts as an insulator Third, it may enter diapause where

its physiological systems are largely inactive and resistant to extremes of temperature

2.4.1 Cold-Hardiness

Cold-hardiness refers to an insect’s ability to adapt to and survive low temperatures

Some insects are “chill-intolerant,” that is, suffer lethal injury even at temperatures above

0◦C Others are “chill-tolerant,” though a period of gradual temperature acclimation

(hard-ening) may be required for tolerance to develop (Bale, 1993, 1996; Sømme, 1999) For

insects in environments that experience temperatures below 0◦C, an additional problem

presents itself, namely, how to avoid being damaged by freezing of the body cells The

formation of ice crystals within cells causes irreversible damage to and frequently death of

an organism (1) by physical disruption of the protoplasm and (2) by dehydration, reduction

of the liquid water content that is essential for normal enzyme activity Insects that

sur-vive freezing temperatures are described as either freezing-susceptible or freezing-tolerant

Freezing-susceptible species are those whose body fluids have a lower freezing point and

may undergo supercooling Freezing-tolerant (= freezing-resistant = frost-resistant) species

are ones whose extracellular body fluids can freeze without damage to the insect

In both groups, two or three types of cryoprotectants (substances that protect against

freezing) are produced Cryoprotectants identified to date fall into three categories: (1)

ice-nucleating agents (proteins), produced only in freezing-tolerant species; (2)

low-molecular-weight polyhydroxyl substances such as proline, glycerol, sorbitol, mannitol, threitol,

su-crose and trehalose; and (3) thermal-hysteresis or antifreeze proteins (Duman and Horwath,

1983; Lee, 1991; Bale, 2002) Typically, insects produce two or more polyhydroxyls This

may be because they are toxic at higher concentrations, an effect that can be avoided by the

use of a multicomponent system

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To appreciate the mode of action of these cryoprotectants, it is necessary to understandthe process of freezing When water is cooled the speed at which individual moleculesmove decreases, and the molecules aggregate As cooling continues there is an increasedprobability that a number of aggregated molecules will become so oriented with respect toeach other as to form a minute rigid latticework, that is, a crystal Immediately this crystal(nucleator) is formed the rest of the water freezes rapidly as additional molecules bind tothe solid frame now available to them Freezing of a liquid does not always depend onthe formation of a nucleator, but can be induced by foreign nucleating agents such as dustparticles or, in the present context, particles of food in the gut or a rough surface such asthat of the cuticle

In freezing-susceptible species cold-hardiness is attained in a two-step process (Bale,2002) In the first step behavioral and physiological activities occur that collectively re-duce the insect’s chance of freezing These may include emptying the gut of food andoverwintering as a non-feeding pupa, hibernating in dry locations, building structures thatprevent contact with moisture, reducing body water content, and increasing fat content.Collectively, these processes may lower the supercooling point to –20◦C In the second steppolyhydroxyls and antifreeze proteins are produced These molecules not only increase theconcentration of solutes in the body fluid so that the freezing point is depressed, but bytheir chemical nature they considerably improve the insect’s supercooling capacity; that

is, the body fluids remain liquid at temperatures much below their normal freezing point.Because of their hydroxyl groups, the cryoprotectants are capable of extensive hydrogenbonding with the water within the body The binding of the water has two important effectswith respect to supercooling First, it greatly reduces the ability of the water molecules toaggregate and form a nucleating crystal, and second, even if an ice nucleus is formed, therate at which freezing spreads through the body is greatly retarded because of the increasedviscosity of the fluid

A remarkable degree of supercooling can be achieved through the use of

cryoprotec-tants In the overwintering larva of the parasitic wasp Bracon cephi, for example, glycerol

makes up 25% of the fresh body weight (representing a 5-Mole concentration) and lowersthe supercooling point of the hemolymph to−47◦C Perhaps a disadvantage to the use

of supercooling as a means of overwintering is that the probability of freezing occurringincreases both with duration of exposure and with the degree of supercooling so that, forexample, an insect might freeze in 1 minute at−19◦C but survive for 1 month at−10◦C.

Thus, to ensure survival an insect must have the ability to remain supercooled at extremetemperatures for significant periods of time, even though the average temperatures to which

it is exposed may be 10◦C to 15◦C higher In other words, it may have to produce muchmore antifreeze in anticipation of those extremes than would be judged necessary on thebasis of the average temperature

The alternative method, employed by freezing-tolerant species, is to permit (be able

to withstand) a limited amount of freezing within the body Freezing must be restricted tothe extracellular fluid, as intracellular freezing damages cells Ice formation in the extracel-lular fluid, which is accompanied by release of heat (latent heat of fusion), will thereforereduce the rate at which the body’s tissues cool as the ambient temperature falls Thus, itwill be to an insect’s advantage to have a large volume of hemolymph (and there is evidencethat this is characteristic of pupae) and to be able to tolerate freezing of a large proportion

of the water within it Two subsidiary problems accompany the freezing-tolerant strategy:

it is necessary (1) to prevent freezing from extending to the cell surfaces (and hence intothe cells) and (2) to prevent damage to cells as a result of dehydration As water in the

661 THE ABIOTIC ENVIRONMENT

extracellular fluid freezes, the osmotic pressure of the remaining liquid will increase, so

that water will be drawn out of the cells by osmosis

Freezing tolerance is generally found in insects living in extremely cold environments

The general strategy used by freezing-tolerant species is to synthesize ice-nucleating

pro-teins in late fall/early winter (i.e., at temperatures above−10◦C) that initiate freezing of

extracellular fluids This early induction of ice formation is advantageous because the rate

of ice formation is less than at lower temperatures, thus allowing water to move out of

cells to maintain osmotic equilibrium and reduce the likelihood of intracellular freezing

(Baust and Rojas, 1985) Through the winter both intra- and extracellular polyhydroxyls

are generated With their ability to bind extensively with water the extracellular

cryoprotec-tants will retard the rate at which freezing spreads, while the intracellular cryoproteccryoprotec-tants

will hold water within cells, to counteract the outwardly pulling osmotic force It has also

been suggested that the cryoprotectants may bind with plasma membranes to reduce their

permeability to water The role of the antifreeze proteins in freezing-tolerant insects is less

clear (Bale, 2002) An early suggestion was that they may protect insects from freezing in

early fall, before the ice-nucleating agents have been synthesized A more likely function

is that they prevent “secondary recrystallization” (refreezing) in the spring, when

polyhy-droxyls are being degraded under the influence of rising temperatures, yet the insect must

be safeguarded against unexpected freezing temperatures

Of interest is the evolutionary selection of glycerol as the dominant cryoprotectant

because in high concentration this molecule is toxic at above-freezing temperatures Storey

and Storey (1991) suggested that at least three factors have been critical First, two molecules

of glycerol are produced from each molecule of its precursor hexose phosphate, important

where colligative properties are concerned Second, the synthesis of a triol

(3-carbon-containing polyol) from a 6-carbon precursor conserves the carbon pool compared to

syn-thesis of 4- or 5-carbon polyols (when the extra carbons are lost as carbon dioxide) Third,

the pathways for glycerol synthesis and breakdown already exist in the fat body as part of

lipid metabolism Insects that use glycerol have biochemical pathways for synthesizing it

in increasing amounts as the temperature falls progressively below 0◦C and, equally, for

degrading it when the temperature increases Such has been shown to be the case in

Pteros-tichus brevicornis, an Arctic carabid beetle that overwinters as a freezing-tolerant adult.

In P brevicornis glycerol synthesis begins when an insect is exposed to a fall temperature

of 0◦C, and by the following December-January the concentration of this molecule may

reach or exceed 30 g/100 ml, sufficient to enable an insect to withstand the –40◦C to –50◦C

temperatures to which it may be exposed at this time Conversely, as temperatures increase

toward 0◦C with the advent of spring, the glycerol concentration falls and the cryoprotectant

disappears from the hemolymph by about the end of April, coincident with the return of

above-freezing average temperatures (Baust and Morrissey, 1977) A comparable situation

is observed in Eurosta solidaginis, a gall-forming fly that overwinters as a freezing-tolerant

third-instar larva The larva has a three-phase cryoprotectant system that comprises

glyc-erol, sorbitol, and trehalose Production of the molecules begins somewhat above 0◦C but

is probably triggered by declining temperatures At temperatures below 0◦C, production of

glycerol and sorbitol is greatly enhanced With the return of warm weather in spring, the

concentration of the three molecules rapidly declines (Baust and Morrissey, 1977)

Cold-hardiness and overwintering diapause (Section 3.2.3) frequently occur together,

and the question of whether the phenomena are physiologically related has been widely

de-bated (Denlinger, 1991) As noted above, studies have correlated the synthesis of

cryopro-tectants with lowered temperatures, and vice versa However, only a handful of examples are

CHAPTER 22

known in which insects exposed to short days (but not low temperatures) develop increasedcold tolerance, presumably by synthesizing cryoprotectants (Saunders, 2002) Denlinger(1991) concluded that, given the diversity of overwintering strategies found among insects,generalization was not possible Thus, in some species cold-hardiness occurs in the absence

of diapause; in others, diapause and cold-hardiness may occur coincidentally or may bephysiologically linked (regulated by the same signals) According to Pullin (1996) there isincreasing evidence that the production of polyhydroxyls is linked to the great suppression

of metabolic rate which accompanies diapause

3 Light

Light exerts a major influence on the ability of almost all insects to survive and multiply

A well-developed visual system enables insects to respond immediately and directly to lightstimuli of various kinds in their search for food, a mate, a “home,” or an oviposition site, and

in avoidance of danger (Chapter 12, Section 7) But light influences the biology of manyinsects in another manner which stems from the earth’s rotation about its axis, resulting

in a regularly recurring 24-hour cycle of light and darkness, the photoperiod.∗ Becausethe earth’s axis is not perpendicular to the plane of the earth’s orbit around the sun, andbecause the orbit varies throughout the year, the relative amounts of light and darkness inthe photoperiod change seasonally and from point to point over the earth’s surface.Photoperiod influences organisms in two ways: it may either induce short-term (diurnal)behavioral responses which occur at specified times in the 24-hour cycle, or bring aboutlong-term (seasonal) physiological responses which keep organisms in tune with changingenvironmental conditions In both situations, however, a key feature is that the organismsthat respond have the ability to measure time In short-term responses the time intervalbetween the onset of light or darkness and commencement of the activity is important Forseasonal responses, the absolute day length (number of hours of light in a 24-hour period) isusually critical, though in some species it is the day-to-day increase or decrease in the lightperiod that is measured In other words, organisms that exhibit photoperiodic responses aresaid to possess a “biological clock,” the nature of which is unknown, though its effects inanimals are frequently manifest through changes in endocrine activity

3.1 Daily Influences of Photoperiod

Various advantages may accrue to members of a species through the performance ofparticular activities at set times of the photoperiod It may be advantageous for some insects

to become active at dawn, dusk, or through the night when ambient temperatures are belowthe upper lethal limit, chances of predation are reduced, and the rate of water loss throughthe cuticle is lessened by the generally greater relative humidity that occurs at these times.For other insects, in which visual stimuli are important, activity during specific daylighthours may be advantageous; for example, food may be available for only a limited part ofthe day, or conversely, other, detrimental factors may restrict feeding to a specific period.For many species it is clearly beneficial for their members to show synchronous activity,

as this will increase the chance of contact between sexes “Activity” in this sense is not

∗ As Beck (1980) noted, some authors use this term to describe the light portion of a light-dark cycle (i.e.,

synonymously with day length).

663 THE ABIOTIC ENVIRONMENT

restricted to locomotion, however For example, in many species of moths, it is by and large

only the males that exhibit daily rhythms of locomotor activity The females are sedentary,

but, in their virgin condition, have daily rhythms of calling (secretion of male-attracting

pheromones) that enable males to locate them

3.1.1 Circadian Rhythms

In a few species daily rhythms of activity are triggered by environmental cues and

are therefore of exogenous origin For example, the activity of the stick insect Carausius

morosus is directly provoked by daily changes in light intensity However, in most species

these rhythms are not simply a response to the onset of daylight or darkness; that is, dawn

or dusk do not act as a trigger that switches the activity on or off Rather, the rhythms are

endogenous (originate within the organism itself) but are subject to modification

(regula-tion) by photoperiod and other environmental factors That the rhythm originates internally

may be demonstrated by placing the organism in constant light or darkness The organism

continues to begin its activity at approximately the same time of the 24-hour cycle, as it

did when subject to alternating periods of light and darkness Because the rhythm has an

approximately 24-hour cycle, it is described as a circadian rhythm When the rhythm is not

influenced by the environment, that is, when environmental conditions are kept constant,

the rhythm is described as “free-running.” When environmental conditions vary regularly in

each 24-hour cycle, and the beginning of the activity occurs at precisely the same time in the

cycle, the rhythm is “entrained.” For example, if a cockroach begins its locomotor activity

2 hours after darkness, this activity is said to be photoperiodically entrained The role of

photoperiod is therefore to adjust (phase set) the endogenous rhythm so that the activity

occurs each day at the same time in relation to the onset of daylight or darkness Though

photoperiod is probably the most important regulator of circadian rhythms in insects, other

environmental factors such as temperature, humidity, and light intensity, as well as

physio-logical variables such as age, reproductive state, and degree of desiccation or starvation may

modify behavior patterns Photoperiodically entrained daily rhythms are known to occur in

relation to locomotor activity, feeding, mating behavior (including swarming), oviposition,

and eclosion, examples of which are given below

Many examples are known of insects that actively run, swim, or fly during a

charac-teristic period of the 24-hour cycle, this activity usually occurring in relation to some other

rhythm such as feeding or mate location In Periplaneta and other cockroaches activity

begins shortly before the anticipated onset of darkness, reaches a peak some 2–3 hours after

dark, and declines to a low level for the remaining period of darkness and during most of the

light period (Figure 22.2A) Drosophila robusta (Figure 22.2B) flies actively during the last

3 hours of the light phase but is virtually inactive for the rest of the 24-hour period Male

ants of the species Camponotus clarithorax are most active during the first few hours of

the light period but show little activity at other times (Figure 22.2C) The above examples

show a well-defined single peak (unimodal rhythm) of activity Other species, however,

have bimodal or trimodal rhythms For example, females of the silver-spotted tiger moth,

Halisidota argentata, show two peaks of flight activity during darkness, the first shortly

after darkness begins, the second about midway through the dark period (Figure 22.3A)

Males of this species, in contrast, have a trimodal rhythm of flight activity (Figure 22.3B)

(Beck, 1980)

Rhythmic feeding activity is apparent in larvae of some Lepidoptera, for example,

H argentata, which feed almost exclusively during darkness Female mosquitoes, too,

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FIGURE 22.2. Locomotor activity rhythms in insects, illustrating photoperiodic entrainment (A) Periplaneta; (B) Drosophila; and (C) Camponotus [From S D Beck, 1968, Insect Photoperiodism By permission of Academic

Press, Inc., and the author.]

FIGURE 22.3. Photoperiodically entrained flight activity in Halisidota argentata (Lepidoptera) [From D K.

Edwards, 1962, Laboratory determinations of the daily flight times of separate sexes of some moths in naturally

changing light, Can J Zool 40:511–530 By permission of the National Research Council of Canada.]

665 THE ABIOTIC ENVIRONMENT

show peaks of feeding activity either at dawn or dusk, or during both of these periods,

though there is some argument with regard to whether feeding activity is endogenous or

simply a direct response to a particular light intensity

Several good examples may be cited to illustrate the importance of photoperiod in

entraining daily endogenous rhythms of mating behavior Many virgin female Lepidoptera

begin to secrete male-attracting pheromones shortly after the onset of darkness and are

maximally receptive to males about midway through the dark period Equally, males show

maximum excitability to these pheromones in the early part of the dark period The males

of certain ant species undertake mating flights at characteristic times within the light period,

typically near dawn or dusk Mosquitoes and other Nematocera form all-male swarms that

females enter for insemination Formation of these swarms, which occurs both at dawn and

at dusk, is an endogenous rhythm, entrained by photoperiod, though temperature and light

intensity are also involved (Beck, 1980)

For some insect species, egg laying has been shown to be a photoperiodically entrained

endogenous rhythm In the mosquitoes Aedes aegypti and Taeniorhynchus fuscopennatus,

for example, oviposition is concentrated in the period immediately after sunset and before

dawn, respectively In other mosquitoes, however, no oviposition rhythm exists and egg

laying appears to be dependent on light intensity

Many examples are known of insects that molt to adults during a characteristic period

of the day Many tropical Odonata exhibit mass eclosion during the early evening and are

able to fly by the following morning Corbet (1963) suggested that this minimizes the effects

of predators such as birds and other dragonflies that hunt by sight In temperate climates

where nighttime temperatures are generally too low for emergence, there may be a switch

to emergence during certain daylight hours In more rigorous climates temperature appears

to override photoperiod∗as a factor regulating emergence, which occurs opportunistically

at any time of the day provided the ambient temperature is suitable (Section 2.3) Species of

Ephemeroptera and Diptera also have daily emergence patterns, which may be associated

with immediate mating and oviposition Though many insect species are known that have a

daily emergence rhythm, for only a few of these, mainly Diptera, is experimental evidence

available that proves the endogenous nature of the rhythm In contrast to the previously

described rhythmic processes, emergence occurs but once in the life of an insect and results

in the appearance of a very different developmental stage, the adult Nevertheless, this single

event, like daily repeated processes, is an endogenous rhythm, entrained by environmental

stimuli, especially photoperiod, that exert their effect in earlier developmental stages For

example, populations of many Drosophila species emerge at maximum rates 1–2 hours

after dawn on the basis of photoperiodic entrainment either in the larval or pupal stage

Thus, if a culture of Drosophila larvae of variable ages is maintained in darkness from the

egg stage except for one brief period of light (a flash lasting as little as 1/2000 of a second

is sufficient) the adults will emerge at regular 24-hour intervals, based on the onset of the

light period being equivalent to dawn; that is, the beginning of the light period serves as the

reference point for entraining the insects’ emergence rhythm (Beck, 1980)

Physiological and molecular studies of light-regulated circadian rhythms have revealed

that, although there is a basic operating system, this may occur in a variety of forms

(Saunders, 2002) The basic system comprises three components: an input pathway, which

includes a photoreceptor; an oscillator (“clock” or pacemaker) that receives the entraining

∗ In the Arctic summer there are, of course, 24 hours of light per day, and photoperiod cannot serve as an entraining

factor for diurnal rhythms.

ff

is located in the lateral neurons (located near the border of the optic lobe and brain) ortheir equivalent, while in moths the clock lies deep in the central part of the brain Outputpathways vary in their nature, depending on the rhythmic activity that is being controlled.For example, in cockroaches the clock connects with interneurons that run to the thoracicganglia where locomotor activity is regulated By contrast, the eclosion rhythm in moths istriggered by eclosion hormone whose release is controlled by the clock in the brain.Though behavioral rhythms such as locomotor activity and eclosion are regulated by

a central clock, it is evident that many other circadian rhythms operate independently;that is, many organs and tissues possess their own clock (Giebultowicz, 2000, 2001) This

is readily shown by separating a structure from the rest of the body and observing that itretains its rhythmicity of function To date, peripheral clocks have been reported for gonads,Malpighian tubules, endocrine glands, epidermis, and some sense organs

Molecular studies, mainly using Drosophila mutants, have identified at least 10 genes

in the central brain oscillator that are involved in circadian locomotor and eclosion rhythms

Two of these genes, period and timeless, and their protein products (PER and TIM,

respec-tively) are responsible for the actual timing mechanism, showing circadian activity and

production, respectively A third gene, cryptochrome, codes for a photosensitive protein

that modulates the action of PER and TIM, thereby resetting the clock Other genes are

on the output pathway (i.e., downstream of the clock), and their gene products induce

manifestation of the circadian rhythm Homologous genes to period have been detected

in the central oscillators of moths and cockroaches, as well as in organs with peripheralclocks (Giebultowicz, 2000), indicating that there may be a common molecular basis forall circadian clocks For further details of the molecular components of circadian clocks,

see Giebultowicz (2000, 2001), Stanewsky (2002), and Zordan et al (2003).

3.2 Seasonal Influences of Photoperiod

Photoperiod affects a variety of long-term physiological processes in insects and, indoing so, allows a species to (1) exploit suitable environmental conditions and (2) surviveperiods when climatic conditions are adverse Some of the ways in which species are enabled

to exploit a suitable environment include being in an appropriate developmental stage as soon

as the suitable conditions appear, and growing or reproducing at the maximum rate whileconditions last Obviously, to survive adverse conditions, members of a species must already

be in an appropriate physiological state when the conditions develop In other words, thephysiological or behavioral changes are induced by cues that are not in themselves adverse.Thus, among the processes known to be affected by photoperiod are the nature (qualitativeexpression) and rate of development, reproductive ability and capacity, synchronized adultemergence, induction of diapause, and possibly cold-hardiness Several of these processesare closely related and are therefore affected simultaneously Other environmental factors,especially temperature, may modify the effects of photoperiod

667 THE ABIOTIC ENVIRONMENT

3.2.1 Nature and Rate of Development

In some species larval growth rates are affected by photoperiod For some species

growth is accelerated under long-day conditions (when there are 16 or more hours of light

in each 24-hour cycle) and inhibited in photoperiods that contain 12 or fewer hours of light;

for other species, the converse is true Often the effect of photoperiod on growth rate is

correlated with the nature of diapause induction; that is, species that grow more slowly

under short-day conditions tend also to enter diapause as a result of short days However, it

should be noted that the growth rate of many species that enter a photoperiodically controlled

diapause is not affected by photoperiod

Exposure to different photoperiods such as occur in different seasons may result in

the development of distinct forms of a species, that is, polyphenism The physiological

(endocrine) basis of polyphenism has been outlined in Chapter 21 (Section 7), and the

present discussion is restricted to a consideration of its induction by photoperiod Sometimes

the forms that develop are so strikingly different that they were described originally as

separate species Beck (1980) cited as an example the European butterfly Araschnia levana,

described originally as two species, A levana and A prorsa, but which is now known to be a

seasonally dimorphic species Caterpillars reared under long-day conditions metamorphose

into the non-diapausing, black-winged (prorsa) form; when they have developed at short day

lengths the caterpillars emerge as red-winged (levana) adults that overwinter in diapause

This example shows a typical feature of most dimorphic Lepidoptera, namely, that one form

is characteristically found in summer and is non-diapausing, whereas the alternate form is

the diapausing, overwintering stage

Photoperiodically influenced polyphenism is also seen in the seasonal occurrence

of normal-winged, brachypterous, and/or apterous forms of species of Orthoptera and

Hemiptera But perhaps the best-known example of the effects of photoperiod on

develop-ment is that of polyphenism in aphids The life cycle of aphid species (see Figure 8.8) is

complex and varied but shows beautifully how an insect takes full advantage of suitable

con-ditions for growth and reproduction A key feature of the life cycle is the occurrence within it

of wingless, neotenic females that reproduce viviparously and parthenogenetically In many

species the offspring are entirely female This combination of features enables aphids to

reproduce rapidly and build up massive populations in the spring and summer when weather

conditions are good and food is abundant As a result of the crowding that results from this

reproductive activity, winged migratory forms develop, and a part of the population moves

on to alternate host plants From these migratory forms several more generations of female

aphids (alienicolae) are produced (again through viviparity and parthenogenesis), which

may be winged or apterous Eventually the alienicolae give rise to winged sexuparae (all

fe-male) that migrate back to the original host plant, and whose progeny may be either winged

males or wingless females (oviparae) These reproduce sexually and lay eggs that pass the

winter in diapause on the host plant The following spring each egg gives rise to a female

in-dividual, the “stem mother” or fundatrix, normally wingless, that reproduces asexually, and

from which several generations of neotenic females (fundatrigeniae) arise There are many

variants of this generalized life cycle, most often through its simplification; that is, one or

more of the life stages is omitted as, for example, in species that do not alternate hosts when

migrants and whose offspring do not appear as distinct forms Indeed, in some species sexual

forms have never been described and reproduction appears to be strictly parthenogenetic

The development of these seasonally occurring aphid forms is influenced by a variety

of environmental factors, including day length Crowding is the major factor that influences

CHAPTER 22

production of summer migrants, whereas the shorter days of late summer and early fallinduce development of sexuparae and oviparae For some species there is a critical day

length for induction of oviparous forms In Megoura viciae (Figure 21.15), for example,

which does not alternate host plants (i.e., it has no migrant form, and the oviparae areproduced directly from fundatrigeniae), the critical day length is 14 hours 55 minutes at

15◦C At greater day lengths continuous production of viviparous, parthenogenetic femalesoccurs; when the day length is below this critical value oviparae are produced

In some species production of males also is induced by short days, though temperature

and maternal age exert a strong influence For example, in the pea aphid Acyrthosiphon pisum male offspring are not produced by young females or by females reared under long-

day conditions Old females reared at short day lengths and temperatures from 13◦C to

20◦C produce a large proportion of males Outside this temperature range the proportion ofmales declines

3.2.2 Reproductive Ability and Capacity

The effects of photoperiod on reproductive processes are almost all indirect, that is,result from other photoperiodically induced phenomena, especially adult diapause (see be-low) By its effect on the nature of development, as in aphids, photoperiod may indirectlymodify the fecundity of a species Beck (1980) noted one example of an apparently direct

effect of photoperiod on fecundity In Plutella xylostella, the diamondback moth, egg

pro-duction in individuals reared under long-day photoperiods averaged 74 eggs/moth, whereasegg production under short-day conditions was only half this value

Occurrence and Nature. Diapause may occur at any stage of the life history, egg,larva, pupa, or adult, though this stage is usually species-specific Only rarely does diapauseoccur at more than one stage in the life history of a species Such is typically the case inspecies that require 2 or more years in which to complete their development For example,

in the cockroach Ectobius lapponicus, which has a 2-year life history, the first winter is

passed as a diapausing egg, the second as a quiescent second- or third-instar larva or as adiapausing fourth-instar larva

Anticipation of the arrival of adverse conditions means that the environmental stimulithat induce diapause must exert their influence at an earlier stage in development Thus,egg diapause is the result of stimuli that affect the parental generation These stimuli act on

669 THE ABIOTIC ENVIRONMENT

the female parent either in the adult stage or, more often, during her embryonic or larval

development In Bombyx mori, for example, the day length experienced by developing

female embryos determines whether or not these insects will lay eggs that enter diapause

Specifically, exposure of embryos to long day lengths results in females that lay diapausing

eggs, and vice versa For B mori good evidence exists for the production of a diapause

hormone by females exposed during embryogenesis to long-day conditions This hormone,

synthesized in the subesophageal ganglion, has as its target organ the ovary, which is caused

to produce diapause eggs Whether this scheme is applicable to the induction of egg diapause

in other species is not known

Diapause may occur at any larval stage, though the instar in which it is present is usually

characteristic for a species In many species it occurs in the final instar and, upon termination,

is immediately followed by pupation In this situation it is referred to as prepupal diapause

In the induction of larval diapause environmental stimuli normally exert their influence at

an earlier larval stage, though species are known in which the environmental stimulus is

given in the egg stage or during the previous generation For example, in the pink bollworm,

Pectinophora gossypiella, the photoperiod experienced by the eggs, as well as that during

larval life, is important in determining whether or not prepupal diapause occurs In Nasonia

vitripennis, a parasitic hymenopteran, induction of larval diapause is dependent on the age

of the female parent at oviposition, as well as on the photoperiod and temperature to which

she is exposed early in adult life

The pupa is the stage in which a large number of species enter diapause The

environ-mental signal that induces diapause is generally given during larval development, though

for some species the influence is exerted in the parental generation In the Chinese oak

silkworm, Antheraea pernyi, for example, the last two larval instars are sensitive to

pho-toperiod, whereas in the horn fly, Haematobia irritans, pupal diapause results when the

female parent has been exposed to short day lengths

Diapause may also occur in adult insects when it is known as reproductive diapause

Either young adults or larval instars are the stages sensitive to environmental stimuli Newly

emerged adult Colorado potato beetles (Leptinotarsa decemlineata), when subjected to

short day lengths, will enter diapause In the boll weevil, Anthonomus grandis, short-day

conditions experienced by larvae will induce diapause in the adult stage

A few eff xamples of intraspecific variation in the diapausing instar are known, especially

in species that occupy a wide geographic range In the pitcher-plant mosquito, Wyeomyia

smithii, northern North American populations overwinter as third-instar larvae whereas

those in the southern United States diapause one instar later

Mansingh (1971) subdivided diapause and the events surrounding it into a number of

phases (Figure 22.4) This arrangement is convenient for a description of the sequence in

which various processes occur, though it must be realized that these phases normally are

not clearly separated in time but merge gradually with one another In the preparatory phase

environmental factors induce changes in metabolic activity in anticipation of diapause,

re-sulting generally in accumulation of reserves, especially fats, but including carbohydrates

and in some hibernating species cryoprotectants During this phase the metabolic rate

re-mains normal Entry into the first phase (induction phase) of diapause is signaled by great

declines in metabolic rate and, in postembryonic stages, activity of the endocrine system

For example, in diapausing Hyalophora cecropia, a saturniid moth, the rate of oxygen

consumption (a measure of metabolic rate) is only about 2% of the prediapause value; in

larval European corn borers (Ostrinia nubilalis), which have a “weak” diapause (see below),

the rate of oxygen consumption falls to about one-quarter of the prediapause level In the

CHAPTER 22

FIGURE 22.4. Phases before, during, and after diapause in overwintering insects Probable (solid arrows) and possible (broken arrows) relationships between the environment, endocrine system, and the various phases

are indicated [From A Mansingh, 1971, Physiological classification of dormancies in insects, Can Entomol.

103:983–1009 By permission of the Entomological Society of Canada.]

induction phase continued production of certain reserves, notably cryoprotectants in wintering species, probably occurs What causes the decline in metabolic rate associatedwith the beginning of diapause is uncertain It may be related to the continued effects of en-vironmental stimuli, or it may result from the changed metabolism of an insect Collectively,the behavioral and physiological changes that occur during the preparatory and inductionphases make up the so-called “diapause syndrome.” The refractory phase (phase of dia-pause development), which follows induction, is perhaps the least understood aspect of thediapause condition Originally, it was proposed that for overwintering insects diapause de-velopment would occur only during a period of exposure to low temperature Such chillingwas thought to be necessary for breakdown of the diapause-inducing or growth-inhibitingsubstances produced earlier, or for reactivation of specific systems (e.g., the endocrine

over-system) important in postdiapause development Tauber et al (1986) and Hodek (2002)

summarized the evidence that, in fact, no such chilling is required; rather, the refractoryphase, like other phases of diapause, is maintained as a result of species-specific tempera-ture and/or photoperiod requirements Of course, under natural conditions, species may besubject to low winter temperatures, but these serve only to prevent premature development,

to prevent breakdown of metabolites important in cold-hardiness and to synchronize diapause development The refractory phase is followed by the activated phase, a period

post-in which post-insects are capable of termpost-inatpost-ing diapause but do not do so because of ing environmental conditions (especially low temperature) Certain authors (e.g., Hodek,2002) consider that once insects reach this stage, when their dormancy is (often) simplytemperature-dependent, they must be considered as being quiescent, that is, no longer indiapause Mansingh (1971), however, pointed out that, although insects in this phase arecapable of continued development, several aspects of their physiology are similar to those ofthe refractory phase, for example, the greatly depressed respiratory rate and presence of cry-oprotectants He believed therefore that activated insects should be considered to be still in

prevail-671 THE ABIOTIC ENVIRONMENT

diapause In Mansingh’s scheme the final phase of diapause is the termination phase, which

occurs when environmental conditions become favorable for development In this phase the

metabolic rate returns to normal, the endocrine system once more becomes active, body

tissues again become capable of nucleic acid and protein synthesis, and any cryoprotectants

present gradually disappear As a result of these changes postdiapause development can

begin

In view of the varying degrees of severity of climatic conditions that insects in different

geographic regions may encounter, it is perhaps not surprising to find that the intensity

(duration and stability) of diapause varies This variability, which is both interspecific

and intraspecific, is manifest as a broad spectrum of dormancy that ranges from a state

virtually indistinguishable from quiescence (“weak” or “shallow” diapause) to one of great

stability (“strong” or “intense” diapause) in which an insect can resist extremely unfavorable

conditions In each situation the strength of diapause is precisely adjusted through natural

selection to provide an insect with adequate protection against the adverse conditions,

yet to continue growth and reproduction as soon as an amenable climate returns Broadly

speaking, insects from less extreme climates show weak diapause [called oligopause by

Mansingh (1971)], in which development may not be completely suppressed; the insects

may continue to grow slowly (and even molt) and feed when conditions permit during

the period of generally adverse climate In weak diapause the induction phase is relatively

short, since the biochemical adjustments that an insect makes in order to cope with the

adverse conditions are relatively simple As a corollary of this, insects that overwinter in

weak diapause are not, for example, very cold-tolerant The refractory phase is short so

that the activated phase is entered relatively soon after diapause has begun, and diapause is

quickly terminated when environmental conditions return to normal Conversely, in strong

diapause, which is the rule in insects from severe climates, there is a lengthy induction

phase, after which development is fully suppressed The refractory phase usually lasts for

several weeks or months, and the activated phase usually does not begin until diapause

is more than half over The termination phase is relatively slow, normally spanning 2 or

3 weeks after the return of suitable climatic conditions Frequently insects that overwinter

in strong diapause are very cold-hardy

Diapause was formerly subdivided into facultative and obligate diapause Facultative

diapause described the environmentally controlled diapause of bivoltine and multivoltine

species (having two or more generations per year) in which the members of certain

genera-tions had no diapause in their life history Obligate diapause referred to the diapause found

in univoltine species (those with one generation per year) in which every member of the

species undergoes diapause It was incorrectly assumed that in univoltine species diapause

was not induced by environmental factors However, experimental work on a number of

univoltine species has revealed that in these species diapause is environmentally controlled

Further study may well demonstrate that this is always the case and render invalid the

distinction between obligate and facultative diapause

Induction, Maintenance, and Termination. Various factors may influence the

course of diapause Photoperiod is especially important in the induction of diapause, though

ambient temperatures, population density, and diet during the preparatory and induction

phases may influence the incidence (proportion of individuals entering diapause) and

in-tensity of dormancy For many species photoperiod is also important, though temperature

plays an increasing role, either alone or in combination with photoperiod, in diapause

maintenance Examples of both hibernating and estivating species that require a specific

photoperiod to terminate diapause are also known