I V E colo gy 22 The Abiotic Environment 1 . Intr oduc t ion The development and reproduction of insects are greatly influenced by a variety of abioti c factors. These factors ma y exert their effects on insects either directl y or indirectl y (throu g h th e i re ff ects on ot h er or g an i sms) an di nt h es h ort- or l on g -term. L igh t, f or exam pl e, ma y exer t an i mme di ate e ff ect on t h eor i entat i on o f an i nsect as i t searc h es f or f oo d ,an d ma yi n d uc e c h anges i nan i nsect’s p h ys i o l ogy i n ant i c i pat i on o f a d verse con di t i ons some mont h s i nt he future. Another abiotic factor to which insects are now routinely subjected (deliberately or otherwise) are p esticides. A p art from the obvious effect of lethal doses of such chemicals, p est i c id es ma yh ave more su b t l e, i n di rect e ff ects on t h e di str ib ut i on an d a b un d ance o f s p ec i es, f or exam pl e, a l terat i on o fp re d ator- p re y rat i os an d , i nsu bl et h a ld oses, c h an g es i n f ecun di ty or rates o fd eve l opment. Under natural conditions organisms are subject to a combination of environmenta l factors, both biotic and abiotic, and it is this combination that ultimatel y determines the di str ib ut i on an d a b un d ance o f as p ec i es. Fre q uent ly ,t h ee ff ect o f one f actor mo di fies t he n orma l res p onse o f an or g an i sm to anot h er f actor. For exam pl e, ligh t, by i n d uc i n gdi a p aus e ( Sect i on 3.2.3), may ma k ean i nsect unrespons i ve to (una ff ecte db y) temperature fl uctua - t ions. As a result, an insect is not harmed by abnormally low temperatures, but nor does i t become active in temporary periods of warmer weather that may occur in the middle of wi nter . 2. Tem p erature 2 .1. Effect on Develo p ment Rate The body temperature of insects, as poikilothermic animals, normally follows closely t he tem p erature of the surroundin g s. Within limits, therefore, metabolic rate is p ro p ortional t oam bi ent tem p erature. Conse q uent ly ,t h e rate o fd eve l o p ment i s i nverse ly p ro p ort i ona l t o tem p erature (F ig ure 22.1). Outs id et h ese tem p erature li m i ts t h e rate o fd eve l o p ment n o longer bears an inversely linear relationship to temperature, because of the deleteriou s e ffects of extreme temperatures on the enzymes that regulate metabolism, and eventually t em p eratures are reached (the so-called u pp er and lower lethal limits) where death occurs. 65 5 656 CHAPTER 22 F I GU RE 22.1 . R elationshi p between tem p erature and rate of develo p ment in e gg so f D rosophila melano g aster (Diptera). The two curves represent different ways of expressing this relationship, each being the reciprocal of the o t h er. [ A f ter H. G. An d rewart h a, 19 6 1 , Intro d uction to t h e Stu d y of Anima l Popu l ation s , Un i vers i t y o f C hi ca go Press. B yp ermission of the author.] W i t hi nt h e range o fli near i ty t h e pro d uct o f temperature mu l t i p li e db yt i me requ i re df o r development 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 the tem p erature fluctuates, p rovided that the fluctuations do not exceed the ran g e of linearit y . Th e tem p erature li m i ts outs id ew hi c hd eve l o p ment ceases an d t h e rate o fd eve l o p ment at ag iv e n temperature vary among spec i es, two seem i ng l yo b v i ous po i nts t h at were apparent l y o verlooked in some early attempts at biological control of insect pests. A predator that, o n the basis of laboratory tests and short-term field trials, had good control potential was found to exert little or no control of the p est under natural conditions. Further stud y showed thi s to b ere l ate d to t h e diff er i n g e ff ects o f tem p erature on d eve l o p ment, h atc hi n g ,an d act i v i t y b etween t h e p est an di ts p re d ator . A b roa d corre l at i on ex i sts b etween t h e temperature li m i ts f or d eve l opment an d t h e habitat occupied by members of a species. For example, many Arctic insects that overwinter in the e gg sta g e com p lete their entire develo p ment (embr y onic + p ostembr y onic) in th e tem p erature ran g e 0 ◦ C to 4 ◦ C ,w h ereas i nt h e Austra li an pl a g ue g rass h o pp er, A ustroicete s c ruc i ata ,d ev e l opment ceases b e l ow 1 6 ◦ C .T hi s means t h at t h e di str ib ut i on o f a spec i es w ill 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 than that antici p ated on the basis of tem p erature data for the followin g reasons: (1) tem p eratur e a d a p tat i on ma y occur, t h at i s, g enet i ca lly diff erent stra i ns ma y evo l ve, eac h ca p a bl eo f s urv i v i n g w i t hi na diff erent tem p erature ran g e; (2) t h e tem p erature li m i ts o fd eve l o p ment may diff er among d eve l opmenta l stages [t hi sa l so serves as an i mportant d eve l opmenta l s ynchronizer in some species (Section 2.3)]; and (3) the insect may have mechanisms for s urvivin g extreme tem p eratures (Section 2.4). 6 5 7 THE A BI O TI C ENVIR O NMEN T Because of the ameliorating effects of the water surrounding them, aquatic insect s are not normall y ex p osed to the tem p erature extremes ex p erienced b y terrestrial s p ecies . F urt h er, b ecause i ce i sa g oo di nsu l ator, d eve l o p ment ma y cont i nue t h rou gh t h ew i nter in some a q uat i cs p ec i es i n tem p erate c li mates, t h ou gh a i r tem p eratures ren d er d eve l o p ment o f terrestrial species impossible. Indeed, through evolution there has been a trend in som e i nsects (e.g., species of Ephemeroptera and Plecoptera) to restrict their period of growth t o the winter, p assin g the summer as e gg sindia p ause. Such s p ecies, whose develo p mental th res h o ld i s usua lly on ly s ligh t ly a b ove 0 ◦ C, a pp ear to g a i nat l east two a d vanta g es f ro m thi s arran g ement. F i rst, t h rou gh t h ew i nter t h ere i sana b un d ance o ff oo di nt h e f orm o f r ott i ng vegetat i on, yet re l at i ve l y li tt l e compet i t i on f or i t. Secon d ,t h ey are re l at i ve l ysa f e from predators (fish) which are sluggish and feed only occasionally at these temperatures ( H y nes, 1970b). Such a life c y cle ma y also allow some s p ecies to inhabit tem p orar y or still b o di es o f water t h at d r y u p or b ecome anaero bi c d ur i n g summer. 2 .2. E ff ect on Act i v i ty and D i spersa l Through its effect on metabolic rate, temperature clearly will affect the activity o f i nsects. Man y of the g eneralizations made above with re g ard to the influence of tem p eratur e o n d eve l o p ment h ave t h e i r p ara ll e li nre l at i on toact i v i t y .T h us, t h ere i s aran g eo f tem p erature wi t hi nw hi c h act i v i ty i s norma l ,t h oug h t hi s range may vary among diff erent stra i ns o f t h e same species. The temperature range for activity is correlated with a species’ habitat; for e xample, in the Arctic, chironomid larvae are normally active in water at 0 ◦ C, and adult s c an fl y at tem p eratures as low as 3.5 ◦ C ( Downes, 19 6 4 ). B y a ff ect i n g an i nsect’s a bili t y to fly tem p erature ma yh ave a mar k e d e ff ect on a s p ec i es’ di spersa l an d ,t h ere f ore, i ts di str ib ut i on. Furt h er, b ecause fli g h t i so f suc hi mportance i n f oo d and/or mate location and, ultimately, reproduction, temperature is of great consequence in d etermining the abundance of species. Insects use various means of raising their bod y t em p erature to that at which fli g ht is p ossible even when the ambient tem p erature is low . Fo r e x am pl e, t h e y ma yb e d ar kly co l ore d so as to a b sor b so l ar ra di at i on, or t h e y ma yb as k o n d ar k sur f aces, aga i nus i ng t h e sun’s h eat. Some mot h san db um bl e b ees b eat t h e i rw i ng s w hile at rest and simultaneously reduce hemolymph circulation in order to increase the t emperature of the thorax (Chapter 17, Section 3.1). A dense coat of hairs or scales covers t he bod y of some insects, which, b y its insulatin g effect, will retard loss of heat g enerate d o ra b sor b e d. I n extreme l yco ld c li mates t h ese p h ys i o l og i ca l , b e h av i ora l , or structura lf eatures ma y n o 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 exem p lified es p eciall y well b y Arctic black flies (Simuliidae: Di p tera). T yp ical adult t em p erate-c li mate s p ec i es are act i ve i nsects t h at mate i n fligh t, an df ema l es ma yfly cons id - e ra bl e di stances i n searc h o f a bl oo d mea l necessar yf or e gg maturat i on. In contrast, f ema l es o f 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 emer g ence. In two s p ecies p artheno g enesis has evolved, thereb y ov e rcom i n g t h e dif ficu l t y o fb e i n gf oun dby ama l e (Downes, 19 6 4). Tem p erature c h an g e, t h rou gh i ts e ff ect on t h eso l u bili t y o f ox yg en i n water, ma y m ar k e dl ymo dif yt h e act i v i ty an d ,u l t i mate l y, t h e di str ib ut i on an d surv i va l o f aquat i c i n- sects. Members of many aquatic species are restricted to habitats whose oxygen conten t r emains relativel y hi g h throu g hout the y ear. Such habitats include rivers and streams that are 658 CHAPTER 22 normally well oxygenated because of their turbulent flow and lower summer temperature , and hi g h-altitude or -latitude p onds and lakes, which g enerall y remain cool throu g h the summer. A l ternat i ve ly , as note di n Sect i on 2.1, t h e lif ec y c l eo f some s p ec i es i s suc h t h a t t h e warmer (ox yg en- d efic i ent) con di t i ons are s p ent i n a res i stant, di a p aus i n g ,e gg sta g e. 2.3. Temperature- S ynchronized Development and Emer g enc e Man y s p ec i es o fi nsects h ave highly s y nc h ron i ze dl arva ld eve l o p ment (a ll l arvae ar e more or l ess att h e same d eve l o p menta l sta g e) an d/ or s y nc h ron i ze d ec l os i on, es p ec i a lly t h ose t h at li ve i n h a bi tats w h ere t h ec li mate i ssu i ta bl e f or growt h an d repro d uct i on f or a li m i te d p eriod each year. Synchronized eclosion increases the chances of finding a mate. It may also increase the p robabilit y of findin g suitable food or ovi p osition sites, or of esca p in gp otentia l p re d ators. S y nc h ron i ze dl arva ld eve l o p ment a l so ma yb ere l ate d to t h eava il a bili t y o ff oo d , an di n some s i tuat i ons i tma yb e necessar yi nor d er to avo id i nters p ec i fic com p et i t i on f or t h e same resource. For certa i n carn i vorous spec i es, suc h as O d onata, sync h ron i ze dd eve l opment may help reduce the incidence of cannibalism among larvae . P erhaps not surprisingly in view of its effects on rate of development and activity, tem p erature i san i m p ortant s y nc h ron i z i n gf actor i nt h e lif eo fi nsects. Its i m p ortance ma y b e ill ustrate dby re f erence to t h e lif e hi stor y o f Coenagrion angu l atum,w hi c h ,a l on g w i t h severa l ot h er spec i es o fd amse lfli es (O d onata: Zygoptera), i s f oun di n or aroun d s h a ll o w p onds on the Canadian prairies (Sawchyn and Gillott, 197 5 ). For these insects the seaso n f or growth and reproduction lasts from about mid-May to mid-October. For the remaining 7 months of the y ear C . angulatum e xists as more or less mature larvae , which , between abou t Novem b er an d A p r il , are encase di n i ce as t h e p on d s f reeze to t h e b ottom. (T h e l arvae t h em- se l ves d o not f reeze, as t h e i ce temperature se ld om f a ll s more t h an a f ew d egrees Ce l s i u s below zero as a result of snow cover. ) In C. a n g u l atu m both larval development and eclosio n are synchronized by temperature. Synchronized development is achieved (1) by means of different tem p erature thresholds for develo p ment in different instars, that is, y oun g er larvae c an cont i nue to g row i nt h e f a ll a f ter t h e g rowt h o f o ld er l arvae h as b een arreste dbyd ecreas- i ng water temperatures, an d (2) b yap h otoper i o di ca ll y i n d uce ddi apause. T h us, samp l e s c ollected in mid-September include larvae of the last seven instars, whereas those from earl y O ctober are composed almost entirely of larvae of the last three instars. Conversely, after the ice melts the followin g A p ril, y oun g er larvae can continue their develo p ment earlier tha n t h e i r more mature re l at i ves, so t h at by m id -Ma y more t h an 90% o f t h e l arvae are i nt h e fina l i nstar. A f ter t h e i rre l ease f rom t h e i ce l arvae m ig rate i nto s h a ll ow water at t h e p on d mar gin wh ose temperature para ll e l st h at o f t h ea i r. Emergence occurs w h en t h ea i r temperature is 2 0 ◦ C to 21 ◦ C (and the water temperature is about 1 2 ◦ C ). It begins normally during the las t week of Ma y and reaches a p eak within 10 da y s. Emer g ence of C . angulatum f o ll ows t h at o f var i ous c hi ronom id san d c h ao b or id s(D ip tera), w hi c hf orm t h ema i n f oo d o f t h ea d u l t d amse lfli es d ur i ng t h e per i o d o f sexua l maturat i on. T h e d eve l opment an d emergence o f other damselfly species that inhabit the same pond are also highly synchronized but occur a t different times of the growing season. This enables the species to occupy the same pond a nd make use of the same resources, y et avoid inters p ecific com p etition. This is discussed f urt h er i nC h a p ter 23 (Sect i on 3.2.1). Th ou gh un p re di cta bl eona d a y -to- d a yb as i s, tem p erature d oes h aveare g u l ar seasona l p attern t h at contro l st h e onset an d term i nat i on o fdi apause i n some spec i es. Temperature i s the primary diapause-inducing stimulus for some subterranean species [e.g., some ground beetles (Carabidae)], wood- and bark-inhabitin g s p ecies, and p ests of stored p roducts that 6 5 9 THE A BI O TI C ENVIRONMEN T live in darkness. It also is the major cue for diapause induction in some insects living n ear the e q uator where chan g es in p hoto p eriod are too small to act as si g nals of seasona l c h an g e(Tau b e r et al. , 198 6 ; Den li n g er, 198 6 ). Tem p erature can a l so exert a stron gi n fl u- e nce on di a p ause an d ot h er ph oto p er i o di ca lly contro ll e dph enomena, as i s di scusse db e l o w ( Section 3.2) . 2 .4. S urvival at Extreme Tem p eratures I n man y tro pi ca l areas c li mat i c con di t i ons are su i ta bl e f or y ear-roun dd eve l o p ment an d r epro d uct i on i n i nsects. In ot h er areas o f t h ewor ld ,t h e year i s di v i s ibl e i nto di st i nct seasons , i n some of which growth and/or reproduction is not possible. One reason for this arrest of g rowth and/or re p roduction ma y be the extreme tem p eratures that occur at this time and ar e p otent i a lly l et h a l to an i nsect. In man yi nstances s h orta g eo ff oo d wou ld a l so occur un d er th ese con di t i ons . To av o id t h e d etr i menta l e ff ects o f per i o d so f mo d erate l y l ow ( d own to f reez i ng) or hi g h t emperature, 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) . Fi rst, t h e lif e hi stor y o f man y s p ec i es i s arran g e d so t h at t h e p er i o d o f a d verse tem p eratur e i s p asse d as t h e i mmo bil e, non- f ee di n g e gg or p u p a. Secon d , p r i or to t h ea d vent o f a d verse con di t i ons [an di ts h ou ld b e rea li ze d t h at t h eto k en st i mu l us t h at tr i ggers t hi s b e h av i or i s not, i n 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 oviposi t i n soil, litter, or p lant tissue, which acts as an insulator. Third, it ma y enter dia p ause wher e i ts phy s i o l o gi ca l s y stems are l ar g e ly i nact i ve an d res i stant to extremes o f tem p erature . 2 .4.1. C old-Hard i ness C o ld - h ar di ness re f ers to an i nsect’s a bili t y to a d a p ttoan d surv i ve l ow tem p eratures . Some i nsects are “c hill - i nto l erant,” t h at i s, su ff er l et h a li n j ur y even at tem p eratures a b ove 0 ◦ C. Ot h ers are “c hill -to l erant,” t h oug h a per i o d o f gra d ua l temperature acc li mat i on ( h ar d - e ning) may be required for tolerance to develop (Bale, 1993, 1996; Sømme, 1999). For i nsects in environments that experience temperatures below 0 ◦ C, an additional problem p resents itself, namel y , how to avoid bein g dama g ed b y freezin g of the bod y cells. The f ormat i on o fi ce cr y sta l sw i t hi nce ll s causes i rrevers ibl e d ama g etoan df re q uent ly d eat h o f an organ i sm (1) b yp h ys i ca ldi srupt i on o f t h e protop l asm an d (2) b y d e h y d rat i on, re d uct i o n o f 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. F reezin g -susce p tible s p ecies are those whose bod y fluids have a lower freezin gp oint and m a y un d er g osu p ercoo li n g . Freez i n g -to l erant ( = f reez i n g -res i stan t = f rost-res i stant) s p ec i es are ones w h ose extrace ll u l ar b o dy fl u id s can f reeze w i t h out d ama g etot h e i nsect . I n b ot h groups, two or t h ree types o f cryoprotectants (su b stances t h at protect aga i ns t freezing) are produced. Cryoprotectants identified to date fall into three categories: (1) ice- nucleatin g a g ents ( p roteins), p roduced onl y in freezin g -tolerant s p ecies; (2) low-molecular- w e igh t p o lyhyd rox yl su b stances suc h as p ro li ne, gly cero l , sor bi to l , mann i to l ,t h re i to l ,su - c rose an d tre h a l ose; an d (3) t h erma l - hy steres i sorant if reeze p rote i ns (Duman an d Horwat h, 1983; Lee, 1991; Ba l e, 2002). Typ i ca ll y, i nsects pro d uce two or more po l y h y d roxy l s. T his m ay be because they are toxic at higher concentrations, an effect that can be avoided by the use of a multicomponent system . 660 CHAPTER 22 To appreciate the mode of action of these cryoprotectants, it is necessary to understand the p rocess of freezin g . When water is cooled the s p eed at which individual molecules move d ecreases, an d t h emo l ecu l es a gg re g ate. As coo li n g cont i nues t h ere i san i ncrease d p ro b a bili t y t h at a num b er o f a gg re g ate d mo l ecu l es w ill b ecome so or i ente d w i t h res p ect t o each 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 t o the solid frame now available to them. Freezin g ofali q uid does not alwa y sde p end on t h e f ormat i on o f a nuc l eator, b ut can b e i n d uce dbyf ore ig n nuc l eat i n g a g ents suc h as d ust p art i c l es or, i nt h e present context, part i c l es o ff oo di nt h e gut or a roug h sur f ace suc h as that of the cuticle. In freezing-susceptible species cold-hardiness is attained in a two-step process (Bale, 2 002). In the first ste p behavioral and p h y siolo g ical activities occur that collectivel y re - d uce t h e i nsect’s c h ance o ff reez i n g .T h ese ma yi nc l u d eem p t yi n g t h e g ut o ff oo d an d ov erw i nter i n g as a non- f ee di n gp u p a, hib ernat i n gi n d r yl ocat i ons, b u ildi n g structures t h at p revent contact w i t h mo i sture, re d uc i ng b o d y water content, an di ncreas i ng f at content . C ollectively, these processes may lower the supercooling point to –20 ◦ C . In the second step p ol y h y drox y ls and antifreeze p roteins are p roduced. These molecules not onl y increase th e c oncentrat i on o f so l utes i nt h e b o dy fl u id so t h at t h e f reez i n gp o i nt i s d e p resse d , b ut by t h e i rc h em i ca l nature t h e y cons id era bly i m p rove t h e i nsect’s su p ercoo li n g ca p ac i t y ;t h a t i s, t h e b o d y fl u id s rema i n li qu id at temperatures muc hb e l ow t h e i r norma lf reez i ng po i nt. B ecause of their hydroxyl groups, the cryoprotectants are capable of extensive hydroge n bondin g with the water within the bod y . The bindin g of the water has two im p ortant effect s w i t h res p ect to su p ercoo li n g .F i rst, i t g reat ly re d uces t h ea bili t y o f t h e water mo l ecu l es to agg re g ate an df orm a nuc l eat i n g cr y sta l ,an d secon d ,even if an i ce nuc l eus i s f orme d ,t he rate at w hi c hf reez i ng sprea d st h roug h t h e b o d y i s great l y retar d e db ecause o f t h e i ncrease d v iscosity of the fluid . A remarkable degree of supercooling can be achieved through the use of cryoprotec - tants. In the overwinterin g larva of the p arasitic was p Bracon ceph i , for exam p le, g l y cero l makes u p 25% of the fresh bod y wei g ht (re p resentin g a 5-Mole concentration) and lowers t h e supercoo li ng po i nt o f t h e h emo l ymp h t o − 47 ◦ C. Per h aps a di sa d vantage to t h eus e of supercooling as a means of overwintering is that the probability of freezing occurring increases both with duration of exposure and with the degree of supercooling so that, for exam p le, an insect mi g ht freeze in 1 minute a t − 19 ◦ Cb ut su r vive fo r1m o n th at − 10 ◦ C . T h us, to ensure surv i va l an i nsect must h ave t h ea bili t y to rema i nsu p ercoo l e d at extrem e temperatures f or s i gn i ficant per i o d so f t i me, even t h oug h t h e average temperatures to w hi c h it is exposed may be 10 ◦ C to 1 5 ◦ C higher. In other words, it may have to produce muc h more antifreeze in anticipation of those extremes than would be judged necessary on th e basis of the avera g e tem p erature . Th ea l ternat i ve met h o d ,em pl o y e dbyf reez i n g -to l erant s p ec i es, i sto p erm i t( b ea ble to w i t h stan d )a li m i te d amount o ff reez i ng w i t hi nt h e b o d y. Freez i ng must b e restr i cte d t o the extracellular fluid, as intracellular freezing damages cells. Ice formation in the extracel - l ular fluid, which is accompanied by release of heat (latent heat of fusion), will therefor e reduce the rate at which the bod y ’s tissues cool as the ambient tem p erature falls. Thus, it w ill b etoan i nsect’s a d vanta g eto h ave a l ar g evo l ume o fh emo ly m ph (an d t h ere i sev id enc e t h at t hi s i sc h aracter i st i co fp u p ae) an d to b ea bl etoto l erate f reez i n g o f a l ar g e p ro p ort i o n of t h e water w i t hi n i t. Two su b s idi ary pro bl ems accompany t h e f reez i ng-to l erant strategy : it is necessary (1) to prevent freezing from extending to the cell surfaces (and hence into the cells) and (2) to p revent dama g e to cells as a result of deh y dration. As water in th e 66 1 THE A BI O TI C ENVIR O NMEN T e xtracellular fluid freezes, the osmotic pressure of the remaining liquid will increase, so t hat water will be drawn out of the cells b y osmosis. Freez i n g to l erance i s g enera lly f oun di n i nsects li v i n gi n extreme ly co ld env i ronments . T h e g enera l strate gy use dbyf reez i n g -to l erant s p ec i es i stos y nt h es i ze i ce-nuc l eat i n gp ro - t eins in late fall/early winter (i.e., at temperatures above − 1 0 ◦ C) that initiate freezing o f e xtracellular fluids. This early induction of ice formation is advantageous because the rate o f ice formation is less than at lower tem p eratures, thus allowin g water to move out of c e ll stoma i nta i n osmot i ce q u ilib r i um an d re d uce t h e lik e lih oo d o fi ntrace ll u l ar f reez i n g ( Baust and Ro j as, 198 5 ). Throu g h the winter both intra- and extracellular p ol y h y drox y l s are generated. With their ability to bind extensively with water the extracellular cryoprotec- t ants will retard the rate at which freezing spreads, while the intracellular cryoprotectant s w ill hold water within cells, to counteract the outwardl yp ullin g osmotic force. It has also b een su gg este d t h at t h ecr y o p rotectants ma ybi n d w i t hpl asma mem b ranes to re d uce t h e i r p ermea bili t y to water. T h ero l eo f t h e ant if reeze p rote i ns i n f reez i n g -to l erant i nsects i s l ess cl ear (Ba l e, 2002). An ear l y suggest i on was t h at t h ey may protect i nsects f rom f reez i ng i n e arly fall, before the ice-nucleating agents have been synthesized. A more likely functio n i s that the yp revent “secondar y recr y stallization” (refreezin g ) in the s p rin g , when p ol y h y- d rox yl s are b e i n gd e g ra d e d un d er t h e i n fl uence o f r i s i n g tem p eratures, y et t h e i nsect must b esa f e g uar d e d a g a i nst unex p ecte df reez i n g tem p eratures . O fi nterest i st h eevo l ut i onary se l ect i on o f g l ycero l as t h e d om i nant 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 o f g l y cerol are p roduced from each molecule of its p recursor hexose p hos p hate, im p ortant wh ere co llig at i ve p ro p ert i es are concerne d . Secon d ,t h es y nt h es i so f atr i o l (3-car b on - c onta i n i ng po l yo l ) f rom a 6 -car b on precursor conserves t h e car b on poo l compare d to syn- t hesis of 4- or 5 -carbon polyols (when the extra carbons are lost as carbon dioxide). Third , t he pathways for glycerol synthesis and breakdown already exist in the fat body as part of li p id metabolism. Insects that use g l y cerol have biochemical p athwa y s for s y nthesizin g it i n i ncreas i n g amounts as t h e tem p erature f a ll s p ro g ress i ve ly b e l ow 0 ◦ Can d ,e q ua lly , f or d egra di ng i tw h en t h e temperature i ncreases. Suc hh as b een s h own to b et h e case in P tero s - tic h us b re v icornis, an A rctic carabid beetle that overwinters as a freezing-tolerant adult . In P. b revicorni s glycerol synthesis begins when an insect is exposed to a fall temperature o f0 ◦ C ,an dby t h e f o ll ow i n g Decem b er-Januar y t h e concentrat i on o f t hi smo l ecu l ema y r eac h or excee d 30 g/ 100 m l ,su f fic i ent to ena bl ean i nsect to w i t h stan d t h e –40 ◦ C t o –50 ◦ C t emperatures to w hi c hi t may b e expose d at t hi st i me. Converse l y, as temperatures i ncreas e t oward 0 ◦ C with the advent of spring, the glycerol concentration falls and the cryoprotectan t d isappears from the hemolymph by about the end of April, coincident with the return of above-freezin g avera g e tem p eratures (Baust and Morrisse y , 1977). A com p arable situation i so b serve din E urosta solidaginis,a g all - f orm i n gfly t h at overw i nters as a f reez i n g -to l eran t thi r d - i nstar l arva. T h e l arva h asat h ree-p h ase cryoprotectant system t h at compr i ses g l yc- e rol, sorbitol, and trehalose. Production of the molecules begins somewhat above 0 ◦ C but i s probably triggered by declining temperatures. At temperatures below 0 ◦ C, production of g l y cerol and sorbitol is g reatl y enhanced. With the return of warm weather in s p rin g , the c oncentrat i on o f t h et h ree mo l ecu l es ra pidly d ec li nes (Baust an d Morr i sse y , 1977). Co ld - h ar di ness an d overw i nter i n gdi a p ause (Sect i on 3.2.3) f re q uent ly occur to g et h er, 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- t ectants with lowered tem p eratures, and vice versa. However, onl y a handful of exam p les are 662 CHAPTER 22 k nown in which insects exposed to short days (but not low temperatures) develop increase d c old tolerance, p resumabl y b y s y nthesizin g cr y o p rotectants (Saunders, 2002). Denlin g e r (1991) conc l u d e d t h at, gi ven t h e di vers i t y o f overw i nter i n g strate gi es f oun d amon gi nsects, genera li zat i on was not poss ibl e. T h us, i n some spec i es co ld - h ar di ness occurs i nt h ea b sence o f diapause; in others, diapause and cold-hardiness may occur coincidentally or may b e p hysiologically linked (regulated by the same signals). According to Pullin (1996) there i s increasin g evidence that the p roduction of p ol y h y drox y ls is linked to the g reat su pp ressio n of meta b o li c rate w hi c h accom p an i es di a p ause. 3. L i ght Ligh texertsama j or i n fl uence on t h ea bili t y o f a l most a ll i nsects to surv i ve an d mu l t iply. A we ll - d eve l o p e d v i sua l s y stem ena bl es i nsects to res p on di mme di ate ly an ddi rect ly to ligh t st i mu li o f var i ous ki n d s i nt h e i r searc hf or f oo d , a mate, a “ h ome,” or an ov i pos i t i on s i te, an d in avoidance of danger (Chapter 12, Section 7). But light influences the biology of man y insects in another manner which stems from the earth’s rotation about its axis, resultin g i nare g u l ar ly recurr i n g 24- h our c y c l eo f ligh tan dd ar k ness, t h e ph oto p er i o d . ∗ Because t h e eart h ’s ax i s i s not p er p en di cu l ar to t h e pl ane o f t h e eart h ’s or bi t aroun d t h e sun, an d b ecause t h eor bi tvar i es t h roug h out t h e year, t h ere l at i ve amounts o fli g h tan dd ar k ness i n the photoperiod change seasonally and from point to point over the earth’s surface. P hoto p eriod influences or g anisms in two wa y s: it ma y either induce short-term (diurnal ) b e h av i ora l res p onses w hi c h occur at s p ec i fie d t i mes i nt h e 24- h our c y c l e, or b r i n g a b out l on g -term (seasona l ) phy s i o l o gi ca l res p onses w hi c hk ee p or g an i sms i n tune w i t h c h an gi n g env i ronmenta l con di t i ons. In b ot h s i tuat i ons, h owever, a k ey f eature i st h at t h e organ i sm s that respond have the ability to measure time. In short-term responses the time interva l b etween the onset of li g ht or darkness and commencement of the activit y is im p ortant. For s easona l res p onses, t h ea b so l ute d a yl en g t h (num b er o fh ours o f ligh t i n a 24- h our p er i o d ) i s u sua lly cr i t i ca l ,t h ou gh i n some s p ec i es i t i st h e d a y -to- d a yi ncrease or d ecrease i nt h e ligh t per i o d t h at i s measure d .Inot h er wor d s, organ i sms t h at ex hibi tp h otoper i o di c responses ar e s aid to possess a “biological clock,” the nature of which is unknown, though its effects i n a nimals are fre q uentl y manifest throu g h chan g es in endocrine activit y . 3.1. Dail y Influences of Photo p eriod V arious advantages may accrue to members of a species through the performance o f p articular activities at set times of the p hoto p eriod. It ma y be advanta g eous for some insects to b ecome act i ve at d awn, d us k ,ort h rou gh t h en igh tw h en am bi ent tem p eratures are b e l ow t h eu pp er l et h a lli m i t, c h ances o fp re d at i on are re d uce d ,an d t h e rate o f water l oss t h rou gh t h e cut i c l e i s l essene db yt h e genera ll y greater re l at i ve h um idi ty t h at occurs at t h ese t i mes. For o ther insects, in which visual stimuli are important, activity during specific daylight h ours may be advantageous; for example, food may be available for only a limited part o f t h e d a y , or converse ly ,ot h er, d etr i menta lf actors ma y restr i ct f ee di n g toas p ec i fic p er i o d . F o r m an y s p ec i es i t i sc l ear ly b enefic i a lf or t h e i r mem b ers to s h ow s y nc h ronous act i v i t y, a st hi sw ill i ncrease t h ec h ance o f contact b etween sexes. “Act i v i ty” i nt hi s sense i s not ∗ A s Bec k (1980) note d , some aut h ors use t hi s term to d escr ib et h e li g h t port i on o f a li g h t- d ar k cyc l e( i .e. , sy non y mousl y with da y len g th). 663 THE A BI O TI C ENVIR O NMEN T r estricted to locomotion, however. For example, in many species of moths, it is by and larg e onl y the males that exhibit dail y rh y thms of locomotor activit y . The females are sedentar y, b ut, i nt h e i rv i r gi n con di t i on, h ave d a ily r hy t h ms o f ca lli n g (secret i on o f ma l e-attract i n g ph eromones) t h at ena bl ema l es to l ocate t h em . 3.1.1. Ci rcad i an Rhythms I na f ew s p ec i es d a ily r hy t h ms o f act i v i t y are tr igg ere dby env i ronmenta l cues an d are t h ere f ore o f exo g enous or igi n. For exam pl e, t h e act i v i t y o f t h est i c ki nsect C arausius m oro s u s i s di rect l y provo k e db y d a il yc h anges i n li g h t i ntens i ty. However, i n most spec i e s t hese rhythms are not simply a response to the onset of daylight or darkness; that is, daw n o r dusk do not act as a tri gg er that switches the activit y on or off. Rather, the rh y thms ar e e n d o g enous (or igi nate w i t hi nt h eor g an i sm i tse lf ) b ut are su bj ect to mo di ficat i on (re g u l a - ti on) by ph oto p er i o d an d ot h er env i ronmenta lf actors. T h at t h er hy t h mor igi nates i nterna lly m ay b e d emonstrate db yp l ac i ng t h e organ i sm i n constant li g h tor d ar k ness. T h e organ i s m continues to begin its activity at approximately the same time of the 24-hour cycle, as i t d id when subject to alternating periods of light and darkness. Because the rhythm has a n a pp rox i mate ly 24- h our c y c l e, i t i s d escr ib e d as a c i rca di an r hy t h m. W h en t h er hy t h m i sno t i n fl uence dby t h eenv i ronment, t h at i s, w h en env i ronmenta l con di t i ons are k e p t constant , th er h yt h m i s d escr ib e d as “ f ree-runn i ng.” W h en env i ronmenta l con di t i ons vary regu l ar l y in e ach 24-hour cycle, and the beginning of the activity occurs at precisely the same time in the c y cle, the rhythm is “entrained.” For example, if a cockroach begins its locomotor activit y 2 hours after darkness, this activit y is said to be p hoto p eriodicall y entrained. The role o f ph oto p er i o di st h ere f ore to a dj ust ( ph ase set) t h een d o g enous r hy t h msot h at t h e act i v i t y o ccurs eac hd a y at t h e same t i me i nre l at i on to t h e onset o fd a yligh tor d ar k ness. T h ou gh photoperiod is probably the most important regulator of circadian rhythms in insects, othe r e nvironmental factors such as temperature, humidity, and light intensity, as well as physio - lo g ical variables such as a g e, re p roductive state, and de g ree of desiccation or starvation ma y m o dify b e h av i or p atterns. P h oto p er i o di ca lly entra i ne dd a ily r hy t h ms are k nown to occur in r e l at i on to l ocomotor act i v i t y , f ee di n g , mat i n gb e h av i or ( i nc l u di n g swarm i n g ), ov ip os i t i on, an d ec l os i on, examp l es o f w hi c h are g i ven b e l ow. M any examples are known of insects that actively run, swim, or fly during a charac- t eristic period of the 24-hour cycle, this activity usually occurring in relation to some other rhy t h m suc h as f ee di n g or mate l ocat i on. I n P eriplaneta a n d ot h er coc k roac h es act i v i t y b e gi ns s h ort ly b e f ore t h e ant i c ip ate d onset o fd ar k ness, reac h es a p ea k some 2–3 h ours a f ter d ar k ,an dd ec li nes to a l ow l eve lf or t h e rema i n i ng per i o d o fd ar k ness an dd ur i ng most o f t he light period (Figure 22.2A). D roso ph i l aro b usta (Figure 22.2B) flies actively during the las t 3 hours of the light phase but is virtually inactive for the rest of the 24-hour period. Male ants of the s p ecies Camponotus clarithora x are most active durin g the first few hours of th e ligh t p er i o db ut s h ow li tt l e act i v i t y at ot h er t i mes (F ig ure 22.2C). T h ea b ove exam pl es s h owawe ll - d efine d s i ng l e pea k (un i mo d a l r h yt h m) o f act i v i ty. Ot h er spec i es, h owever , h ave bimodal or trimodal rhythms. For example, females of the silver-spotted tiger moth , Ha l isi d ota ar g entata , show two peaks of flight activity during darkness, the first shortl y after darkness be g ins, the second about midwa y throu g h the dark p eriod (Fi g ure 22.3A). Ma l es o f t hi ss p ec i es, i n contrast, h aveatr i mo d a l r hy t h mo f fligh t act i v i t y (F ig ure 22.3B ) ( Bec k , 1980) . R h yt h m i c f ee di ng act i v i ty i s apparent i n l arvae o f some Lep id optera, f or examp l e , H. ar g entata , which feed almost exclusively during darkness. Female mosquitoes, too , [...]... the Colorado potato beetle, L decemlineata, and the pink bollworm, P gossypiella In FIGURE 22. 5 Different types of diapause incidence-day length relationships in insects (A) Long-day; (B) short-day; (C) short-day-long-day; and (D) long-day-short-day The hatched line in Figure 22. 5A indicates that in some long-day species diapause incidence is less than 100% at very short day lengths [From S D Beck,... continuous Such insects are said to show a short-day response (Figure 22. 5B) The European corn borer, O nubilalis, and the imported cabbage worm, Pieris brassicae, have a short-day-long-day response to photoperiod; that is, the incidence of diapause is low at short and long day lengths, but high at intermediate day lengths (14–16 hours of light per day) (Figure 22. 5C) The ecological significance of such a... physiologically dormant condition (diapause) At below-freezing temperatures insects may also become freezing-tolerant, that is, capable of withstanding freezing of their extracellular fluids, or, when they are freezing-susceptible, become supercooled In both arrangements, polyhydroxyl cryoprotectants, thermal-hysteresis proteins, and (for freezing-tolerant species) ice-nucleating proteins are important In species... insects, development is continuous at day lengths below the critical value (usually about 12 hours) In short-day-long-day insects, development is continuous at short and long day lengths, but at intermediate day lengths (about 14–16 hours of light per day) the incidence of diapause is high Long-day-short-day insects develop continuously within a narrow range of day lengths (16–20 hours of light per day)... migratory behavior (McNeil et al., 1995; Dingle, 2001) In most insects JH stimulates egg development (Chapter 19, 679 THE ABIOTIC ENVIRONMENT 680 CHAPTER 22 FIGURE 22. 7 Interactions leading to population outbreaks in the spruce budworm (Choristoneura fumiferana) Terms in parentheses relate to populations under non-outbreak conditions [From P W Price, Insect Ecology, 2nd ed Copyright C 1984 by John Wiley and... 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... Lepidoptera behave in the opposite manner, namely, show a long-day-short-day response to photoperiod (Figure 22. 5D) All photoperiods except those with 16–20 hours of light per day induce diapause Again, however, the ecological value of such a response is uncertain The precise value of the critical day length for a species varies with latitude (Figure 22. 6) For example, the sorrel dagger moth, Acronycta rumicis,... 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 669 THE ABIOTIC ENVIRONMENT 670 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,... results in a 1-hour difference in the critical day length At extreme values the effects of temperature may overcome those of photoperiod with reference to induction of diapause In long-day insects exposure to constant high temperature may completely prevent diapause induction regardless of photoperiod Conversely, in short-day insects high temperature induces diapause, even under long-day conditions... length Most insects studied to date show a long-day response to photoperiod (Figure 22. 5A) That is, when reared under long-day conditions, they show continuous development, whereas at short day lengths diapause is induced Between these extremes is a critical day length at which the incidence of diapause changes abruptly Examples of insects that show a long-day response are the Colorado potato beetle, . suc h as that of the cuticle. In freezing-susceptible species cold-hardiness is attained in a two-step process (Bale, 2 002). In the first ste p behavioral and p h y siolo g ical activities occur. concerne d . Secon d ,t h es y nt h es i so f atr i o l (3-car b on - c onta i n i ng po l yo l ) f rom a 6 -car b on precursor conserves t h e car b on poo l compare d to syn- t hesis of 4- or 5 -carbon. charac- t eristic period of the 24-hour cycle, this activity usually occurring in relation to some other rhy t h m suc h as f ee di n g or mate l ocat i on. I n P eriplaneta a n d ot h er coc k roac h es