23 The Biotic En v ironment 1 . Intr oduc t ion T his chapter will deal with the biotic environment of insects, which is composed of all other or g anisms that affect insects’ abilit y to survive and multipl y . In other words, the interaction s of insects with other or g anisms (of the same and other species) will be discussed. Food i s th e most o b v i ous an di m p ortant bi ot i c f actor, an di nsects are i nvo l ve di naw id es p ectrum o f trop hi cre l at i ons hi ps w i t h ot h er organ i sms, b ot hli v i ng an dd ea d .Ast h ema j or i ty o f i nsects f ee d on p l ant mater i a li n one f orm or anot h er, t h e y are k e y components i nt h e fl ow of ener gy throu g h the ecos y stem. However, other interactions are known that, thou g h not as easil y reco g nized as feedin g , are nonetheless important re g ulators of insect distribution an d a b un d ance . 2. Food and Tro p h i c Relat i onsh ip s I nsects have evolved diverse feedin g habits that allow them to exploit virtuall y ever y naturally occurring organic substance. Among their adaptations are specialized ingestiv e an ddi gest i ve systems, t h ea bili ty to d etox if yorp h ys i ca ll y avo id tox i ns pro d uce db yt he h ost, mutua li st i cre l at i ons hi ps b etween t h e i nsect an d m i croor g an i sms, an d lif e- hi stor y strate g ies that result in temporal avoidance of resource-poor situations (includin g those resultin g from interspecific competition) or times when the host’s toxins are abundant. T hus, insects participate in an array of trophic interactions as herbivores, predators, parasites, paras i to id s, d etr i t i vores, an d prey i n b ot h terrestr i a l an df res h water ecosystems (F i gures 23. 1 an d 23.2). Foo d may b ean i mportant li m i ter o fi nsect popu l at i on growt h ; i t may a l so a ff ect t he distribution and the dispersal of species over time (Price, 1997) . 2 .1. Quantitative As p ect s T h oug h t h e amount o ff oo d ava il a bl em i g h t b e cons id ere d as an i mportant regu l ator o f i nsect a b un d ance, i t h as b een f oun di n natura l commun i t i es t h at popu l at i ons d o not norma ll y u se more t h an a sma ll f ract i on o f t h e tota l ava il a bl e f oo d .T hi s i spr i mar ily b ecause ot h er 6 91 6 9 2 CHAPTER 23 F I GU RE 23.1. A n example of a food web in a terrestrial ecosystem, showing the importance of insects. [From P. W. Pr i ce, T h e concept o f t h e ecosystem, i n: Eco l ogica l Entomo l og y (C. B. Hu ff a k er an d R. L. Ra bb ,e d s.) . C op y r igh t  CC 1984 by Jo h nW il e y an d Sons, Inc. Repr i nte dby perm i ss i on o f Jo h nW il e y an d Sons, Inc.] c omponents of the environment especiall y weather but includin g , for example, predators, parasites, and pathogens, usually have a significant adverse effect on growth and reproduc - t i on. Ot h er f eatures o fi nsects may, h owever, b e i mportant i nt hi s regar d . Many spec i es , e spec i a ll yp l ant f ee d ers, are po l yp h agous. T h us, w h en t h e pre f erre df oo d p l ant i s i n li m - i ted quantit y , alternate choices can be used. Amon g endopter yg otes, larvae and adults of a species ma y eat quite different kinds of food, and in some species such as mosquitoes the f ood of the adult female differs from that of the adult male . Two si tuat i ons may occur i nw hi c h t h e quant i ty o ff oo dli m i ts i nsect di str ib ut i on an d a b un d ance. In t h e fi rst, t h ere i snoa b so l ute s h ortage o ff oo d , b ut on l y a proport i on o f t he tota li sava il a bl e to a spec i es. T h us, t h ere i ssa id to b e a “re l at i ve s h orta g e” o ff oo d .Var i ou s reasons ma y account for the food not bein g available. (1) The food ma y be concentrated 6 93 THE BI O TI C ENVIRONMEN T F IGURE 23.2. A n example of a food web in a freshwater ecosystem, showing the importance of insects. [From P .W . Pr i ce, T h e concept o f t h e ecos y stem, i n : E co l ogica l Entomo l ogy ( C. B. Hu ff a k er an d R. L. Ra bb ,e d s. ). Cop y ri g h t  CC 1984 b y John Wile y and Sons, Inc. Reprinted b y permission of John Wile y and Sons, Inc. ] w ithin a small area so that it is available to relativel y few insects. As an interestin g exampl e of this Andrewartha (1961) cited the Shinyanga Game-Extermination Experiment in Eas t Africa in which, over the course of about 5 years, the natural hosts of tsetse flies wer e v i rtua ll y exterm i nate d over an area o f a b out 800 square m il es. At t h een d o f t hi s per i o d on e small elephant herd and various small un g ulates remained in the g ame reserve. However , almost no tsetse flies could be found, despite the fact that, collectivel y , the mammals tha t remained could suppl y enou g h blood to feed the entire ori g inal population of flies. Th e di str ib ut i on o f t h e f oo d was now so sparse t h at t h ec h ance o ffli es o b ta i n i ng a mea l wa s pract i ca ll yn il . (2) T h e f oo d may b e ran d om l y di str ib ute db ut diffi cu l tto l ocate. T h us, on ly a f ract i on o f t h e i n di v id ua l s searc hi n g ever fi n df oo d . Suc hi s pro b a bly t h es i tuat i on i n man y parasitic or h y perparasitic species whose host is buried within the tissues of plants or othe r 6 94 CHAPTER 23 animals. (3) A proportion of the food ma y occur in areas that for other reasons are no t n ormall y visited b y the consumer so that, in effect, it is not available. In the second situation, food ma y become a limitin g factor in population g rowth whe n a spec i es’ num b ers are not k ept i nc h ec kb yot h er i n fl uences, espec i a ll y natura l enem i es. T hi s may h appen, f or examp l e, w h en a spec i es i s acc id enta ll y trans f erre d (o f ten as a resu l t o f human activit y ) from its ori g inal environment to a new g eo g raphic area where its natural e nemies are absent. Under these conditions, the population ma yg row unchecked, and its final size is limited onl y b y the amount of food available. Occasionall y , even in a species ’ n atura lh a bi tat, f oo d may li m i t popu l at i on growt h , f or examp l e, w h en weat h er con di t i on s are f avora bl e f or d eve l opment o f a spec i es b ut not f or d eve l opment o f t h ose organ i sms t h a t pre y on or paras i t i ze i t. 2.2. Q ual i tat i ve Aspects T he nature of the food available ma y have strikin g effects on the survival, rate of g rowth, and reproductive potential of a species, and much work has been done on insect s i nt hi s regar d . For examp l e, o f t h e i nsect f auna assoc i ate d w i t h store d pro d ucts, t h esaw - toot h e d gra i n b eet l e , Or y zaep h i l us surinamensi s , can surv i ve on l yon f oo d sw i t h a hi g h c ar b o hyd rate content suc h as fl our, b ran, an dd r i e df ru i t, w h ereas spec i es o f sp id er b eet l es , Pt i nus spp ., and flour beetles , T r iboliu m spp., have no such carboh y drate requirement an d are consequentl y cosmopolitan, occurrin g in animal meals and dried y east, in addition t o p l ant pro d ucts. For some p h ytop h agous i nsects, a com bi nat i on o f p l ants o f diff erent ki n ds appears necessary f or surv i va l an d /or norma l rates o fj uven il e d eve l opment. In t h em i grator y g rass h opper, M e l anop l us san g uinipe s , f or examp l e, a sma ll er percenta g eo fi nsects surv i ve f rom hatchin g to adulthood, and the development of those that do survive is slower when the g rasshoppers are fed on wheat (Tr i t i cum aest i vum) alone com p ared with wheat p lus fli xwee d (Descurainia Sop h ia)o r d an d e li on ( T a r axacum officinale rr ) (Pickford, 1962) . B ot h t h e rate o f egg pro d uct i on an d t h e num b er o f eggs pro d uce d may b e mar k e dl y a ff ecte dby t h e nature o f t h e f oo d ava il a bl e. Man y common fli es, f or examp l e, spec i es o f M usc a , C alli p hor a , an d L ucilia , ma y survive as adults for some time on a diet of carbo- h y drate. However, for females to mature e gg s a source of protein is essential. Pickfor d ( 1962) showed that M . san g u i n i pe s f ema l es f e d a di et t h at i nc l u d e dwh eat an d wild mustar d ( Bra ss ica k a b e r ) o r wheat and flixweed produced far more eggs ( 5 79 and 467 eggs pe r f ema l e, respect i ve ly )t h an f ema l es f e d on w h eat (243 e gg s / Ɋ ), w ild mustar d (431 e gg s/ Ɋ ), o r flixweed (249 e gg s / Ɋ ), alone. These differences in e gg production resulted lar g el y fro m v ariations in the duration of adult life, thou g h differences in rate of e gg production were also evident. For exam p le, p ercent survival of females fed wheat p lus mustard after 1, 2 , and 3 months was 93%, 6 0%, and 13%, respectively. These females produced, on average, 8 .4 e gg s/ f ema l e per d a y .T h e correspon di n gfig ures f or f ema l es f e d on w h eat a l one wer e 8 7%, 27%, and 0% survival over 1, 2, and 3 months, respectivel y , and 4. 6 e gg s/female per da y . The metabolic basis for these differences was not determined . 3 .In sec t-Pl a nt Int e r ac t io n s 3 .1. Herbivore s Th ou gh i nsects f ee d on p l ants f rom a ll o f t h ema j or taxonom i c g roups, t h e g reates t n umber of herbivorous species feed on an g iosperms with which the y have been coevolvin g 6 9 5 THE BI O TI C ENVIRONMEN T since the Cretaceous period (Chapter 2, Section 4.2). All parts of a plant ma y be exploite d as a result of the activities of g razin g , suckin g , and borin g insects. As mi g ht be anticipated in view of the len g th of time over which this coevolution has occurred, some of the rela - ti ons hi ps b etween h er bi vorous i nsects an d ang i osperms are extreme l y i nt i mate an d re fi ne d , th oug h essent i a ll yt h ere l at i ons hi ps h ave a common t h eme. Insects ga i n energy ( f oo d )a t th e expense o f p l ants, w h ereas p l ants attempt to d e f en d t h emse l ves (conserve t h e i r ener gy ) or at least to obtain somethin g in return for the ener gy that insects take from them. Thou g h t he theme remains constant throu g h time, the relationships themselves are alwa y s chan g in g as a resu l to f natura l se l ect i on. Insects str i ve to i mprove t h e i r energy-gat h er i ng e ffi c i enc y (most o f ten b y concentrat i ng on energy i n a part i cu l ar f orm an df rom a restr i cte d sourc e an db y spec i a li zat i on o f t h e met h o d use d to co ll ect t h e energy) w hil ep l ants concurrent l y improve their defenses. Most authors, for example, Price (1997) view this relationship as “constant warfare” between insects and p lants, which forms the basis of their coevolu- t ion. Other authors such as Owen and Wiegert (1987) believe that herbivory is a form of mutua li sm. T h ey po i nt out t h at, i n ana l ogy w i t h prun i ng, mow i ng, an d s i m il ar act i v i t i e s carr i e d out b y h umans, a f requent e ff ect o fi nsects graz i ng on new l y f orme d p l ant t i ssues i s t o stimulate the plant to produce more branches and, eventuall y , more reproductive struc- t ures and seed; in other words, the plant is makin g an adaptive, mutualistic response to th e h erbi v ore. T h e most common met h o d use db yp l ants as d e f ense aga i nst i nsects (an d ot h er h er - bi vorous an i ma l s) i s pro d uct i on o f tox i c meta b o li tes. P l ants pro d uceaw id e array o f suc h chemicals in secondar y metabolic pathwa y s (i.e., those not used for g eneration of ma - j or components such as proteins, nucleic acids, and carboh y drates). Particular t y pes o f secondar y plant compounds are commonl y restricted to specific plant families, for exam- p l e, g l ucos i no l ates i n Brass i caceae (cruc if ers), car d eno lid es (ma i n l y car di ac g l ycos id es) in Asclepiadaceae (milkweeds), and cucurbitacins in Cucurbitaceae (Panda and Khush, 199 5 ; Sc h oon h ove n et al. , 1998). Moreover, t h e compoun d so f ten accumu l ate w i t hi n spec ifi ct i s- sues or areas of the plant, for example, trichomes (terpenes), the wax la y er (phenolics) , vacuoles (alkaloids), and seeds (non-protein amino acids) (Berna y s and Chapman, 1994) . Th e repro d uct i ve parts o f p l ants, w hi c h represent concentrate d stores o f energy, are es - pec i a ll y attract i ve to h er bi vores an d o f ten serve as a s i n kf or secon d ary meta b o li tes. For examp l e, Hypericum per f oratum ( K l amat h wee d ) pro d uces t h e tox i cqu i none h yper i c i n . T he concentration of h y pericin is 3 0 µ g / g wet wei g ht in the lower stem, 70 µ g / g in the upp er stem, and 500 µ g / g in the flower (Price, 1997). T y picall y , the toxins are chemicall y combined with sugars, salts, or proteins to render them inactive while in storage. When th e p l ant t i ssue i s d amage d , enzymes re l ease t h e tox i n f rom i ts con j ugate, a ll ow i ng a l oca li ze d e ff ect at t h es i te o f t h e woun d (Bernays an d C h apman, 1994). The evolutionar y ori g in of these secondar y metabolites remains a matter of specula- t ion. An earl y view was that the chemicals arose as waste products of a plant’s primar y metabolism, and the plant, being unable to excrete the molecules, simply retained them wi t hi n i ts t i ssues. T hi s id ea i s now cons id ere d un lik e l yg i ven t h e hi g hl y comp l ex nature o f some o f t h ese compoun d san d ,t h ere f ore, t h e amount o f energy requ i re df or t h e i r synt h es i s . A more lik e ly poss ibili t yi st h at or igi na lly t h e meta b o li tes were s i mp ly s h ort- li ve di nterme- d iates in normal biochemical pathwa y s within plants and/or provided a means of storin g chemical ener gy for later use b y the plant. In other words, the ori g inal function(s) of these compoun d s may h ave b een unre l ate d to t h e occurrence o fh er bi vores. An examp l eo f suc ha compoun d m i g h t b en i cot i ne pro d uce db yt h eto b acco p l an t ( Nicotian a spp.). Ra di o i sotope stu di es h ave s h own t h at, a l t h ou gh a b out 12% o f t h e ener gy trappe di np h otos y nt h es i s i s use d 6 9 6 CHAPTER 23 f or nicotine production, the nicotine has a relativel y short half-life, 40% of it bein g converted to other metabolites (possibl y su g ars, amino acids, and or g anic acids) within 10 hours . T hus, animals adapted to feedin g on plants that produce toxins will be at a consid- e ra bl ea d vantage over an i ma l st h at are not. Among h er bi vores, i nsects s h ow t h e greatest a bili ty to cope w i t h t h e tox i ns. In part, t hi sar i ses f rom t h e enormous per i o d o f t i me ove r whi c h coevo l ut i on o fi nsects an d p l ants h as occurre d , b ut i t i sa l so re l ate d to i nsects’ high reproductive rate and short g eneration time, which facilitate rapid adaptation to chan g es i n the host plant. Throu g h evolution, man y insect species have not onl y developed increas- i ng to l erance to a h ost p l ant’s tox i ns b ut are now attracte db yt h em. In ot h er wor d s, suc h i nsects l ocate f oo d p l ants b yt h e scent or taste o f t h e i r tox i csu b stance an df requent l yar e restr i cte d to f ee di ng on suc h p l ants. For examp l e, certa i n fl ea b eet l es, Phyll otreta spp., an d c abba g e worms , Pieris spp., feed exclusivel y on plants such as Cruciferae that produce g lucosinolates (mustard oil). Colorado potato beetles, L eptinotarsa decemlineata, and var- i ous hornworms, M anduca spp., feed only on Solanaceae, the family that includes potato ( S o l anum tu b erosum) (pro d uces so l an i ne), to b acco ( N i cot i an a s pp.) (n i cot i ne), an dd ea dly nightshade ( Atropa belladonna ( ( ) (atrop i ne) (Pr i ce, 1997) . T he method most often used to overcome the potentiall y harmful effects of thes e c hemicals is to convert them into non-toxic or less toxic products. Especiall y important in such conversions is a group of enzymes known as mixed-function oxidases (polysubstrate m onooxygenases), w hi c h ,ast h e i r name i n di cates, cata l yze a var i ety o f ox id at i on react i ons ( Sc h oon h oven et a l ., 1998). T h e enzymes are l ocate di nt h em i crosome f ract i on ∗ of ce ll san d o ccur in particularl y hi g h concentrations in fat bod y and mid g ut. Perhaps unsurprisin g l y ,it is these same enz y mes that are often responsible for the resistance of insects to s y nthetic insecticides (Cha p ter 1 6 , S ection 5.5.) . Some i nsects are a bl eto f ee d on potent i a ll y d angerous p l ants as a resu l to f e i t h er tempora l or spat i a l avo id ance o f t h e tox i c mater i a l s. For examp l e, t h e lif e hi story o f t he winter moth , Op ero p htera brumata , is such that the caterpillars hatch in the earl y sprin g a nd feed on y oun g leaves of oak ( Q uercu s spp.), which have onl y low concentrations of tannins, molecules that complex with proteins to reduce their digestibility. Though weather c on di t i ons are su i ta bl ean df oo di sst ill apparent l yp l ent if u ll ater i nt h e season, a secon d g enerat i on o f w i nter mot h s d oes not d eve l op b ecause b yt hi st i me l arge quant i t i es o f tann i ns a re present in the leaves. Spatial avoidance is possible for man y Hemiptera whose delicate s uctorial mouthparts can b y pass localized concentrations of toxin in the host plant. Some a phids feed on senescent foliage where the concentration of toxin is less than that of younger, meta b o li ca ll y act i ve t i ssue (Pr i ce, 1997) . P r i ce (1997) propose d t h at at l east f our a d vantages may accrue to an i nsect a bl eto f eed on potentiall y toxic plants. First, competition with other herbivores for food will be much reduced. Second, the food plant can be located easil y . Related to this, as member s o f a species will tend to a gg re g ate on or near the food plant, the chances of findin ga mate w ill b e i ncrease d .T hi r d , if an i nsect i sa bl e to store t h e i ngeste d tox i nw i t hi n i ts t i ssues, i t may ga i n protect i on f rom wou ld - b e pre d ators. Many examp l es o f t hi sa bili t y a re k nown, espec i a lly amon g Lep id optera (B l um, 1981; N i s hid a, 2002). T h us, most o f t h e insect fauna associated with milkweeds are able to store the cardenolides produced b y these p lants. These substances, at sublethal levels, induce vomitin g in vertebrates. Other well- k nown examp l es are pyrro li z idi ne a lk a l o id s sequestere db y arct iid mot h s, an d cucur bi tac i ns ∗ Th em i crosome f ract i on i so b ta i ne db y diff erent i a lhi g h -spee d centr if ugat i on o fh omogen i ze d ce ll san d cons i sts o ff ra g mente d mem b ranes o f en d op l asm i c ret i cu l um, r ib onuc l eoprote i ns, an d ves i c l es. 6 9 7 THE BI O TI C ENVIRONMEN T accumulated b y cucumber beetles. In Lepidoptera the chemicals are accumulated b y the caterpillar sta g e and are transferred at metamorphosis to the adult. Further, in some species t he female endows her e gg s with the toxin so that the y , too, are protected (Blum and Hilker, 2002). Most i nsect spec i es t h at sequester tox i ns f rom t h e i r h ost p l ant are aposemat i ca ll y ( b r i g h t l yan ddi st i nct l y) co l ore d ,a f eature common l y i n di cat i ve o f a di staste f u l organ i s m an d one t h at ma k es t h em stan d out a g a i nst t h e b ac kg roun d o f t h e i r h ost p l ant. On samp li n g such insects, a would-be vertebrate predator discovers their unpalatabilit y and quickl y learns to avoid insects havin g a particular color pattern. Remarkabl y , a few insect predators h ave evo l ve d to l erance to t h ep l ant-pro d uce d tox i ns store db yt h e i r i nsect prey an d are , th emse l ves, unpa l ata bl etopre d ators f urt h er up t h e f oo d c h a i n(E i sner e ta l ., 1997). T h e f ourt h a d vantage to b ega i ne db yto l erance to t h ese p l ant pro d ucts i s protect i on aga i ns t patho g enic microor g anisms. For example, cardiac g l y cosides in the hemol y mph of the lar ge milkweed bu g , O ncopeltus fasciatus,h av ea s tron g antibacterial effect. Also, cucurbitacin s sequestered by the adult female cucumber beetle, D iabrotica undecimpunctata howardi , prov id e ant if unga l protect i on f or h er eggs an d o ff spr i ng (Ta ll am y e ta l. , 1998). T h ec h anne li ng o f energy i nto pro d uct i on o f tox i c or repe ll ent su b stances i st h e mos t often used method b y which plants ma y obtain protection, thou g h others are known. A few plants expend this “ener gy of protection” on formation of structures that prevent or d eter feeding, or even harm would-be feeders. For example, passion flowers (Passi fl or a ad enopo d a )h av em i nute h oo k e dh a i rs t h at gr i pt h e i ntegument o f caterp ill ars attempt i n g t o f ee d on t h em. T h e h a i rs b ot hi mpe d e movement an d tear t h e i ntegument as t h e caterp il - lars stru gg le to free themselves so that the insects die from starvation and/or desiccation (Gilbert, 1971). Le g uminous plants have evolved a variet y of ph y sical (as well as chemical ) mechanisms to p rotect their seeds from Bruchidae ( p ea and bean weevils). These includ e pro d uct i on o f gum as a l arva penetrates t h e see d po d so t h at t h e i nsect i s d rowne d or i ts movements hi n d ere d , pro d uct i on o f a fl a k ypo d sur f ace t h at i ss h e d , carry i ng t h e weev il ’s e gg sw i t hi t, as t h epo db rea k s open to expose i ts see d s, an d pro d uct i on o f po d st h at open explosivel y so that seeds are immediatel y dispersed and, therefore, not available to females t hat oviposit directl y on seeds (Center and Johnson, 1974) . 3 .2. In sec t-Pl a nt M u t ua l is m Not all insect-plant relationships are of the “constant warfare” t y pe j ust discussed. For a lar g e number of insect and plant species, an interaction of mutual benefit has evolved. Thus , some insects live in close association with plants, protecting them in return for food. For example, the bull’s-horn acacias ( A cacia ( ( s pp.) are h ost to co l on i es o f ants (Pseu d om y rme x spp.) t h at li ve w i t hi nt h eswo ll en, h o ll ow st i pu l ar t h orns an df ee d on nectar (pro d uce din petioles) and protein (in Beltian bodies at the tips of new leaves) (Fi g ure 23.3). In return, t he a gg ressive ants g uard the plants a g ainst herbivores and suppress the g rowth of nearb y, potentially competitive plants by chewing their growing tips (H¨olldobler and Wilson, 1990). A mutua li st i cre l at i ons hi po f a very diff erent ki n di st h at i nw hi c h t h e h ost supp li e s f oo d to i nsects, i n return f or w hi c h t h e i nsects prov id et h e transport system f or di spersa l o f po ll en, see d s, an d spores. T h ou gh t h e i r i mportance as po lli nators f or high er p l ants h as b ee n extensivel y studied ( K evan and Baker, 1983, 1999; Schoonhove n et al. , 1998 ) , it must be emphasized that some insects are essential for spore dispersal in some mosses and man y fungi (see Chapter 16, Section 4.2.4), as well as transporting seeds of angiosperms. The success ( i mportance) o fi nsects as po lli nators compare d w i t h po lli nators f rom ot h er group s suc h as bi r d san db ats i s presuma bly a resu l to f t h e i r muc hl on g er evo l ut i onar y assoc i at i o n 6 98 CHAPTER 23 F IGURE 23.3 . Mutua li sm b etween b u ll ’s- h orn acac i aan d ants. (A) Acac i a l ea f an d tw i gs h ow i ng extra fl ora l n ectar y , h o ll ow t h orns, an dl ea fl ets w i t h Be l t i an b o di es at t i ps; (B) en l ar g e d v i ew o fh o ll ow t h orn w i t h entrance hole of ant nest; and (C) close-up view of Beltian bodies and ant visitor. [A, redrawn from W. M. Wheeler, 1910, A nts. T h eir Structure, Deve l opment an d Be h aviour.Co l um bi aUn i vers i ty Press. B, C, p h otograp h s courtesy o f D an L. Per l man.] w ith plants. Most of the modern insect orders were well established b y the time the earliest flowerin g plants appeared about 225 million y ears a g o. Thus, insects were able to g ai n a cons id era bl e h ea d start as p o lli nators over bi r d san db ats, t h e ear li est f oss il recor d s f or w hich date back about 1 5 0 and 60 million years, respectively (Price, 1997). To a c hi eve e ff ect i ve cross-po lli nat i on, two i mportant f actors must b eta k en i nto con- sideration in an evolutionar y sense. First, plants must produce precisel y the ri g ht amount o f 6 9 9 THE BI O TI C ENVIRONMEN T F IGURE 23.3. ( Continue d ) nectar to ma k ean i nsect’s v i s i t energet i ca ll y wort h w hil e, yet st i mu l ate v i s i ts to ot h er p l ants , an d secon d ,p l ants o f t h e same spec i es must b e eas il y recogn i ze db yan i nsect. I f too muc h ener gy i sma d eava il a bl e by eac h p l ant, t h en i nsects nee d v i s i t f ewer p l ants an d t h e extent o f cross-pollination is reduced. If a plant produces too little food (to ensure that an insect will visit man y plants), there is a risk that the insect will seek more accessible sources of food, N atural selection determines the precise amount of energy that each plant must offer to a n i nsect, an d t hi s amount d epen d sonanum b er o ff actors. T h e amount o f energy ga i ne db ya n i nsect d ur i ng eac h v i s i ttoa fl ower i sre l ate d to b ot h quant i ty an d qua li ty o f ava il a bl e f oo d . T hus, until recentl y , it was considered that man y adult insects obtained their carboh y drat e re q uirements from nectar and their p rotein re q uirements from other sources such as p ollen , v e g etative parts of the plant (as a result of larval feeding), or other animals. Baker an d B a k er (1973) s h owe d , h owever, t h at t h e nectar o f many p l ants conta i ns s i gn ifi cant amount s o f am i no ac id s , so t h at i nsects can concentrate t h e i re ff orts on nectar co ll ect i on. T hi s not onl y increases the extent of cross-pollination b y inducin g more visits to flowers, but ma y also lead to econom y in pollen production, as pollen becomes less important as food for t he insects. The amount of nectar p roduced is a function of the number of flowers p er p lant . Hence, f or p l ants w i t h a num b er o ffl owers bl oom i ng sync h ronous l y, i t i s i mportant t h at eac hfl ower pro d uces on l y a sma ll amount o f nectar an d po ll en, so t h at an i nsect must v i s i t other plants to satisf y its requirements . More nectar is produced b y plant species whose members t y picall yg row some distanc e apart, so that it is still ener g eticall y worthwhile for an insect species to concentrate on these p l ants. Re l ate d to t hi s, i nsects t h at f orage over greater di stances are l arger spec i es suc h as b ees, mot h s, an db utter fli es w h ose energy requ i rements are hi g h .W h en nectar i s pro d uce d i n l ar g e amounts, i t i st y p i ca lly access ibl eon ly to l ar g er i nsects t h at are stron g enou gh to g ain entr y into the nectar-producin g area or have sufficientl y elon g ate mouthparts. Thi s ensures that nectar is not wasted on smaller insects lackin g the abilit y to carr y pollen t o ot h er mem b ers o f t h e pl ant s p ec i es. Temperature a l so a ff ects t h e amount o f nectar pro d uce d ,as i t i sre l ate d to t h e energ y expen d e dbyi nsects i n fligh tan d to t h et i me o fd a y an d /or season. For examp l e, i n temperate re g ions and/or at hi g h altitudes, flowers that bloom earl y in the da y or at ni g ht, or earl y 7 00 CHAPTER 23 o r late in the season, when temperatures ma y not be much above freezin g , must provide a lar g e enou g h reward to make fora g in g profitable at these temperatures. An alternative to production of lar g e amounts of nectar b y individual flowers is for plants that bloom at lowe r temperatures to grow i n hi g hd ens i ty an dfl ower sync h ronous l y (He i nr i c h an d Raven, 1972) . B eyon d a certa i n di stance b etween p l ants, h owever, t h e amount o f nectar t h at an i nsect requ i res to co ll ect at eac h p l ant ( i nor d er to rema i n“ i ntereste d ” i nt h at spec i es) excee d st h e m aximum amount that the p lant is able to p roduce. Thus, the p lant must ado p t a differen t strate gy . Amon g orchids, for example, about one half of the species produce no nectar, but r e l yonot h er met h o d s to attract i nsects, espec i a ll y d ecept i on b ym i m i cry. T h e fl ower s m ay resem bl e (1) ot h er nectar-pro d uc i ng fl owers, (2) f ema l e i nsects so t h at ma l es ar e attracte d an d attempt pseu d ocopu l at i on, (3) h osts o fi nsect paras i to id s, or (4) i nsects t h a t are subsequentl y attacked b y other territorial insects. These somewhat risk y methods of attractin g insects are offset b y the evolution of hi g hl y specific pollen receptors (so that onl y pollen from the correct species is acquired) and a high degree of seed set for each pollination ( Pr i ce, 1997) . It i s i mportant f or b ot h p l ants an di nsects t h at i nsects v i s i t mem b ers o f t h e same p l ant species. The chances of this occurrin g are g reatl y increased (1) when the plant species has a restricted period of bloom, in terms of both season and/or time of da y ; (2) where members o f a species grow in aggregations, though this is counterbalanced by a restriction of gen e fl ow if po lli nators wor k w i t hi n a part i cu l ar p l ant popu l at i on; an d (3) w h en t h e fl owers ar e e as il y recogn i ze db yan i nsect w hi c hl earns to assoc i ateag i ven p l ant spec i es w i t hf oo d . Reco g nition is achieved as a result of flower morpholo gy (and related to this is accessibilit y o f the nectar and pollen), color, and scent. The advanta g e to an insect species when its m embers can reco g nize particular flowers is that, throu g h natural selection, the species wil l b ecome more e ffi c i ent at gat h er i ng an d ut ili z i ng t h e f oo d pro d uce db yt h ose fl owers . Th e d egree o fi n fl uence t h at t h ese var i a bl es exert i s man if est as a spectrum o fi nt i macy b etween p l ants an d t h e i r i nsect po lli nators. At one en d o f t h e spectrum, t h ep l ant- i nsec t relationship is non-specific; that is, a variet y of insect species serve as pollinators for a variet y o f plants. Neither insects nor flowers are especiall y modified structurall y or ph y siolo g icall y. A tt h e oppos i te extreme, t h ere l at i ons hi p i s suc h t h atap l ant spec i es i spo lli nate db ya s i ng l e i nsect spec i es. Structura lf eatures o f t h epo lli nator prec i se l y comp l ement fl ower m orp h o l ogy; t h ep l ant’s bl oom i ng per i o di s sync h ron i ze d w i t h t h e lif e hi story an ddi urna l activit y of the insect; and, where present, nectar is produced in exactl y the ri g ht quantit y and qualit y to satisf y the insect’s requirements . Harvester ants (those that use seeds as food) are important seed dispersers, resulting f rom acc id enta ll oss o f t h e see d sast h ey transport t h em b ac k to t h e nest or b y f a il ure to use t h e see d s b e f ore t h ey germ i nate. T hi s act i v i ty part i a ll y compensates f or t h e d amage cause d to the plant b y the ants’ seed predation. This mutualistic relationship has been taken to a new l evel of sophistication b y m y rmecochorous plants, which produce attractive appenda g es ( elaiosomes) on their seeds and chemicals to induce the ants to trans p ort the seeds without d amag i ng t h em (F i gure 23.4). T h ee l a i osomes are r i c hi n nutr i ents an df orm t h e f oo d o f t h e ants, w hil et h e see di tse lf i s di scar d e d .T h oug h examp l es o f myrmecoc h ory are k nown w or ld w id e, i t seems to b eap h enomenon o fh a bi tats t h at are nutr i ent-poor (espec i a lly t h os e deficient in phosphorus and potassium), notabl y the dr y schleroph y ll re g ions of Australia an d S outh Africa where more than 90% of the 3100 known species of m y rmecochorous plant s are f oun d .It h as b een specu l ate d t h at p l ants i nt h ese h a bi tats use myrmecoc h ory b ecause e nerget i ca ll y i t i s f ar l ess expens i ve t h an t h e pro d uct i on o f t h e l arger f ru i ts pre f erre db y v ertebrates ( Beattie, 198 5 ;H¨olldobler and Wilson, 1990 ) . [...]... ENVIRONMENT 714 CHAPTER 23 Bacteria known to be naturally pathogenic in insects can be arranged in two groups, the non-spore-formers and the spore-formers.∗ Included among the non-spore-forming bacteria is Serratia marcescens, varieties of which attack a range of insect species and whose presence is recognized by the reddish color of the dead host Outbreaks of S marcescens are common in high-density laboratory... (1984) Aspects of insect-plant interactions are reviewed by Schoonhoven et al (1998) [general] and in the volumes edited by Wallace and Mansell (1975) [biochemical interactions], Gilbert and Raven (1975) [insect-plant coevolution], Strong et al (1984) [insect-plant communities], Beattie (1985) and Huxley and Cutler (1991) [ant-plant interactions], and Panda and Khush (1995) [host-plant resistance to insects]... bees, though a non-spore-former, Streptococcus pluton, is the causative agent The remaining species are secondary pathogens or saprophytes The spore-formers are the most important group from the point of view of epizootics and for their potential importance in biological control, largely because they remain viable for a considerable time outside their host Further, some species (the so-called crystalliferous... virtually extinct, being restricted to a few small areas along the coast However, A lingnanensis was ineffective as a control agent of red scale in the inland citrus-growing areas around San 705 THE BIOTIC ENVIRONMENT 706 CHAPTER 23 FIGURE 23. 5 Changes in the distribution of Aphytis chrysomphali, A lingnanensis, and A melinus in southern California between 1948 and 1965 [After P DeBach and R A Sundby,... dispersal of the pathogen are greater under these conditions On occasion, an epizootic may develop at low host density, as a result of widely dispersed but long-lived pathogens that remain from a previous high-density outbreak Even at high host-population density, an epizootic may not develop if the host population has a discontinuous distribution and/or poor mobility The importance of the environment,... highly synchronously between the last week of May and mid-June Sexual maturation takes about 1 week and the oviposition period extends to the end of July Females lay eggs in the submerged parts of floating plants Embryogenesis is direct and requires less than 3 weeks; half-grown larvae may be collected before the end of July and mature larvae by mid-September Included in Type B are three species of Lestes:... Strepsiptera, and so-called “parasitic” Hymenoptera (Chapter 10, Section 7) A parasitoid may be defined as “an insect that requires and eats only one animal in its life span, but may be ultimately responsible for killing many” (Price, 1997, p 141) Typically, a female parasitoid deposits a single egg or larva on each host, which is then gradually eaten as the offspring develops Adult parasitoids are free-living... should their sporangia be ingested because the sporangia include, in addition to a spore, a crystalline structure, the parasporal body that contains various toxic proteins (the δ-endotoxins) Two of the better known, spore-forming, non-crystalliferous bacteria are Bacillus cereus, which has been isolated from a range of host species, and B larvae, which is the cause of American foulbrood in bee larvae Only... massive numbers (109 per corpse) to be released as the corpse decays or is eaten Some viruses are relatively short-lived outside the insect host and their survival from year to year requires that at least some members of the host population survive Others, 715 THE BIOTIC ENVIRONMENT 716 CHAPTER 23 such as NPVs and CPVs, are able to survive outside the host for a considerable time under suitable conditions... better-known NPVs and because they are relatively slow-acting 5.2.4 Fungi Studies on entomogenous fungi, including their potential as control agents, tend to be overshadowed by the enormous volume of work being carried out on bacteria and viruses However, the first attempt at microbial control (by Metschnikoff in 1879 against larvae of the wheat cockchafer, Anisoplia austriaca) used the green-muscardine . exam- p l e, g l ucos i no l ates i n Brass i caceae (cruc if ers), car d eno lid es (ma i n l y car di ac g l ycos id es) in Asclepiadaceae (milkweeds), and cucurbitacins in Cucurbitaceae (Panda and. of ma - j or components such as proteins, nucleic acids, and carboh y drates). Particular t y pes o f secondar y plant compounds are commonl y restricted to speci c plant families, for exam- p l e,. a species will in- creasin g l y compete with each other for such resources as oviposition sites, overwinterin g 7 04 CHAPTER 23 sites, restin g places, and, occasionall y , food. Such competition