Entomology 3rd edition - C.Gillott - Chapter 18 ppt

1 8 N itrogenous Excretion an d Sa l tan d W ater Ba l ance 1 . Introduct i o n E nzymatically controlled reactions occur at the optimum rate within a narrow range of physical conditions. Especially important are the pH and ionic content of the cell fluid, a s t hese factors readil y affect the active site on an enz y me. As the conditions existin g within ce ll san d t i ssues are necessar ily d e p en d ent on t h e nature o f t h e fl u id t h at b at h es t h em— i n i nsects, t h e h emo l ymp h — i t i st h eregu l at i on o f t hi s fl u id t h at i s i mportant. By regu l at i o n i s meant the removal of unwanted materials and the retention of those that are useful , t o maintain as nearly as possible the best cellular environment. Regulation is a functio n of the excretor y s y stem and is of g reat im p ortance in insects because the y occu py such var i e dh a bi tats an d ,t h ere f ore, h ave diff erent re g u l ator y re q u i rements. Terrestr i a li nsects l os e w ater b y evaporat i on t h roug h t h e i ntegument an d resp i ratory sur f aces an di nt h e process o f n itrogenous waste removal. Brackish-water and saltwater forms also lose water as a result of osmosis across the integument; in addition, they gain salts from the external medium. Insect s i nhabitin g fresh water g ain water from and lose salts to the environment. The p roblem o f osmore g u l at i on i s com pli cate dby an i nsect’s nee d to remove n i tro g enous waste p ro d ucts o f meta b o li sm, w hi c hi n some i nstances are ver y tox i c. T hi s remova l uses b ot h sa l ts an d w ater, one or both of which must be recovered later from the urine. 2 . Excretor ySy stem s 2 . 1 . Malp i gh i an Tubules—Rectu m The Malpighian tubules and rectum, functioning as a unit, form the major excretor y s y stem in most insects. Details of the rectum are g iven in Cha p ter 16, Section 3.4, and onl y th e structure o f t h etu b u l es i s d escr ib e dh ere . T h e bli n dly en di n g tu b u l es, w hi c h usua lly li e f ree ly i nt h e h emocoe l ,o p en i nto t h e alimentary canal at the junction of the midgut and hindgut (Figure 18.1A). Typically they e nter the gut individually but may fuse first to form a common sac or ureter that leads i nto the g ut. Their number varies from two to several hundred and does not a pp ear to be 5 37 53 8 C HAPTER 18 F IGURE 18.1 . (A) Excretory system o f Rhodnius. Only one Malpighian tubule is drawn in full; (B) junction of p rox i ma l an ddi sta l se g ments o f aMa lpighi an tu b u l eo f R h o d nius . P art o f t h etu b u l e h as b een cut awa y to s h ow t he c ellular differentiation; (C, D) sections of the wall of the distal and p roximal se g ments, res p ectivel y , of a tubule; a n d (E) t i po f Ma l p i g hi an tu b u l eo f A pi s t os h ow trac h eo l es an d sp i ra l musc l es. [A, B, E, a f ter V. B. W i gg l eswort h , 196 5, Th e Princip l es o f Insect P hy sio l og y ,6 t h e d ., Met h uen an d Co. B yp erm i ss i on o f t h e aut h or.C,D, f ro m V. B. Wi gg lesworth and M. M. Salt p eter, 1962, Histolo gy of the Mal p i g hian tubules in Rhodnius p rolixus S tal . (Hem i ptera), J. Insect Physiol. 8 :299–307. By perm i ss i on o f Pergamon Press Lt d . ] c losely related to either the phylogenetic position or the excretory problems of an insect . M alpighian tubules are absent in Collembola, some Diplura, and aphids; in other Diplura, P rotura, and Stre p si p tera there are p a p illae at the j unction of the mid g ut and hind g ut. W i t h t h etu b u l es are assoc i ate d trac h eo l es an d , usua lly , musc l es (F ig ure 18.1E). T h e l atter ta k et h e f orm o f a cont i nuous s h eat h , h e li ca l str i ps, or c i rcu l ar b an d san d are s i tuate d o utside the basal lamina. They enable the tubules to writhe, which ensures that differen t p arts of the hemolymph are exposed to the tubules and assists in the flow of fluid along th e tubules. Atu b u l e i sma d eu p o f as i n gl e l a y er o f e pi t h e li a l ce ll s, s i tuate d on t h e i nner s id eo fa b asa ll am i na (F ig ure 18.1B–D). In man y s p ec i es w h ere t h etu b u l es h ave on ly a secretor y f unction (Section 3.2) the histology of the tubules is constant throughout their length and basically resembles that of the distal part of the tubule of R h o d nius ( Figure 18.1C). The inner (a p ical) surface of the cells takes the form of a brush border (microvilli). The oute r ( b asa l ) sur f ace i sa l so extens i ve ly f o ld e d . Bot h o f t h ese f eatures are t ypi ca l o f ce ll s i nvo l ve d i nt h e trans p ort o f mater i a l san d serve to i ncrease enormous ly t h e sur f ace area across w hi c h transport can occur. Numerous m i toc h on d r i a occur, espec i a ll ya dj acent to or w i t hi nt he f olded areas, to supply the energy requirements for active transport of certain ions acros s the tubule wall. In many species various types of intracellular crystals occur which are 53 9 N ITR O GEN O U S EX C RETION A ND S ALT AND WA TER B A L A NC E presumed to represent a form of storage excretion (Section 3.3). Adjacent cells are closely a pp osed near their a p ical and basal mar g ins, thou g h not necessaril y elsewhere. I n some i nsects (e. g ., Rh o dniu s ), two di st i nct zones can b e seen i nt h eMa lpighi an t u b u l e(F ig ure 18.1C, D). In t h e di sta l (secretor y ) zone t h ece ll s p ossess l ar g e num b ers o f c l ose l y pac k e d m i crov illi , b ut very f ew i n f o ldi ngs o f t h e b asa l sur f ace. M i toc h on d r i aar e located near or within the microvilli. In the proximal (absorptive) part of the tubule the cells p ossess fewer microvilli, y et show more extensive inva g ination of the basal surface . T h em i toc h on d r i a are corres p on di n gly more even ly di str ib ute d .Int h e fli e s Dacu s an d Droso p hil a , w h ere p a i rs o f Ma lpighi an tu b u l es un i te to f orm a ureter p r i or to j o i n i n g t he g ut, t h eu l trastructure o f t h e ureter resem bl es t h at o f t h e prox i ma l part o f t he R hod niu s t ubule, suggesting that the ureter may be a site of resorption of materials from the urine . Y e t o ther species have even more complex Malpighian tubules in which up to four dis- ti nct re gi ons ma yb e di st i n g u i s h e d on hi sto l o gi ca l or u l trastructura lg roun d s. On t h e b as i s o f t h e structura lf eatures o f t h e i rce ll s, t h ese re gi ons h ave b een d es ig nate d as secretor y or a b sorpt i ve, t h oug hi t must b e emp h as i ze d t h at p h ys i o l og i ca l ev id ence f or t h ese propose d functions is largely lacking. For a survey of insects whose tubules show regional differen - t iation and a discussion of tubule function in such species, see Jarial and Scudder (1970). Acr yp tone p hridial arran g ement of Mal p i g hian tubules is found in larvae and adult s o f man y Co l eo p tera, some l arva l H y meno p tera an d Neuro p tera, an d near ly a ll l arva l L ep id optera (F i gure 18.2). Here t h e di sta l port i on o f t h eMa l p i g hi an tu b u l es i sc l ose l y apposed to the surface of the rectum and enclosed within a perinephric membrane. The sys- t em is particularly well developed in insects living in very dry habitats, and in such species i ts function is to im p rove water resor p tion from the material in the rectum (Section 4.1) . 2 .2. Other Excretor y Structures Even in insects that use the rectum as the primary site of osmoregulation, the ileum m a y nonetheless be a site for water or ion resor p tion. In other s p ecies where the rectum i s u n i m p ortant i n osmore g u l at i on, serv i n g on ly to store ur i ne an df eces p r i or to ex p u l s i on, t h e il eum o f ten ta k es on t hi sro l e . I na f ew i nsects t h e l a bi a l g l an d s may f unct i on as excretory organs. In apterygotes t h a t lack Malpighian tubules the glands can accumulate and eliminate dyes such as ammonia carmine and indigo carmine from the hemolymph, but there is no evidence that they can d eal similarl y with nitro g enous or other wastes. The labial g lands of saturniid moths excret e co pi ous amounts o ffl u id j ust p r i or to emer g ence f rom t h e cocoon, an di tma y we ll be th at t h epr i mary f unct i on o f t h eg l an d s i store d uce h emo l ymp h vo l ume an dh ence b o d y w eight, which, in such large flying insects, needs to be kept as low as possible. The midgu t of silkmoth larvae actively removes potassium from the hemolymph, thus protecting the t issues from the ver y hi g h concentration of p otassium ions p resent in the leaves eaten b y th ese i nsects . I na f ew i nsects i ta pp ears t h at t h eMa lpighi an tu b u l es, t h ou gh p resent, pl a y no p art i n nitrogenous excretion. In Peri pl aneta americana , for example, uric acid is not found i n t he tubules but does occur in small amounts in the hindgut, which may excrete it directly from the hemol y m p h. In P. a mericana much uric acid is stored in urate cells in the fat bod y , a n d t h ema j or f orm o f excrete d n i tro g en i nt hi ss p ec i es i s ammon i a. How t hi s reac h es t h e hi n dg ut l umen i n P. am e r i can a i s unc l ear. However, i nt h e fl es hfly S arcopha g a bullat a , ammon i a, t h epr i mary excretory pro d uct, i s act i ve l y secrete d as ammon i um i ons i nto t h e lumen across the anterior hindgut wall. 5 4 0 C HAPTER 18 F I GU RE 18 . 2 . Cr yp tone ph r idi a l arran g ement o f Ma lpighi an tu b u l es i n Tene b rio l arva. (A) Genera l a pp earance. N ote that only three of the six tubules are drawn fully and that in reality the tubules are much more convolute d an dh ave more b oursou fl ures t h an are s h own; (B) cross sect i on t h roug h poster i or reg i on o f cryptonep h r idi a l sy stem; (C) d eta il so f a l e p to ph ra g ma; an d (D) di a g ram ill ustrat i n gp ro p ose d mo d eo f o p erat i on o f s y stem. Solid arrows indicate movements of potassium, hollow arrows indicate movements of water. Numbers indicate o smot i c concentrat i on (measure d as f reez i ng-po i nt d epress i on) o ffl u id s i n diff erent compartments. [A f ter A. V. G r i mstone, A. M. Mu lli n g er, an d J. A. Ramsa y ,19 6 8, Furt h er stu di es on t h e recta l com pl ex o f t h e mea l wor m Tenebri o m o lit o r L . (Coleoptera, Tenebrionidae) , P hilos. Trans. R. S oc. Lond. S er. B 25 3 :343–382. By permissio n of t h eRoya l Soc i ety, Lon d on, an d Pro f essor J. A. Ramsay.] 54 1 N ITR O GEN O U S EXCRETION A ND S ALT AND WA TER B A L A NC E I n males of some species of cockroaches, for example, B l atte ll a germanic a ,a consi d - e rable amount of uric acid (as much as 5% of the live wei g ht of the insect) is found in the u tr i cu li ma j ores ( p art o f t h e accessor y re p ro d uct i ve gl an d com pl ex). T h eur i cac id b ecomes part o f t h ewa ll o f t h e spermatop h ore an di s, i n a sense, “excrete d ” d ur i ng copu l at i on. 3 . Nitrogenous Excretio n 3 .1. The Nature of Nitrogenous Wastes I nn i trogenous wastes structura l comp l ex i ty, tox i c i ty, an d so l u bili ty go h an di n h an d . The simplest form of waste (ammonia) is highly toxic and very water-soluble. It contains a h i g h p ro p ortion of h y dro g en that can be used in p roduction of water. It is g enerall y found a s th ema j or excretor yp ro d uct, t h ere f ore, on ly i nt h ose i nsects t h at h ave ava il a bl e l ar g e amount s o f water, f or exam pl e, l arvae an d a d u l ts o ff res h water s p ec i es. Nonet h e l ess, exce p t i ons are k nown, t h e b est examp l es b e i ng t h e l arvae o f meat-eat i ng fli es an d P . a m e r i cana un d e r certain dietary regimes. Generally, however, in insects, as in other terrestrial organisms , w ater must be conserved, and more com p lex nitro g enous wastes are p roduced, which are b ot hl ess tox i can dl ess so l u bl e. In t h ee gg an dp u p a l sta g et h e p ro bl em i s accentuate d b ecause water l ost cannot b ere pl ace d ,an d n i tro g enous wastes must rema i n i nt h e b o dy i nt h ea b sence o f a f unct i ona l excretory system. Most i nsects, t h en, excrete t h e i r wast e n itrogen as uric acid. This is only slightly water-soluble, relatively non-toxic, and contains a smaller proportion of hydrogen compared with ammonia . However, ur i cac id i s not t h eon ly f orm o f n i tro g enous waste. Usua lly traces o f ot h e r m ater i a l s (es p ec i a lly t h ere l ate d com p oun d sa ll anto i nan d a ll anto i cac id ) can b e d etecte d , an di n many spec i es one o f t h ese h as b ecome t h e pre d om i nant excretory pro d uct (Burse ll , 1967). Urea is rarely a major constituent of insect urine, usually representing less than 10% of the nitrogen excreted. Traces of amino acids can be found in the excreta of many insects , but t h e i r p resence s h ou ld b ere g ar d e d as acc id enta ll oss rat h er t h an d e lib erate excret i o n by an i nsect (Burse ll ,19 6 7). On ly occas i ona lly h as t h e excret i on o fp art i cu l ar am i no ac id s b een aut h ent i cate d ; f or examp l e, t h ec l ot h es mot h Tine o l a a n d t h e carpet b eet le A tta g enus e xcrete large amounts of the sulfur-containing amino acid cystine. Although in tsetse flies u ric acid is the primary excretory product, two amino acids, arginine and histidine, are i m p ortant com p onents of the urine. These make u p about 10% of the p rotein amino acids i n h uman- bl oo d ; b ecause t h e i rn i tro g en content i s high , i t i s p ro b a bly uneconom i ca l t o d egra d et h em, an d t h ey are t h ere f ore excrete d unc h ange d (Burse ll ,19 6 7). T h eam i no ac ids voided in honeydew by plant-sucking Hemiptera must be considered as largely fecal and not m etabolic waste products. Because of the large amount of water taken in by aphids, it has b een su gg ested that the y mi g ht p roduce ammonia as their nitro g enous waste. Indeed, uri c ac id, a ll anto i n , an d a ll anto i cac id cannot b e d etecte di nt h e i r excreta. However , ammon i a m akes u p onl y 0. 5 % of the total nitro g en excreted, which has led to the su gg estion that it i s used (and detoxified) by symbiotic bacteria in mycetomes (Chapter 16, Section 5 .1.2) . Table 18.1 contains selected examples to show the variety of nitrogenous wastes produced by insects . As can b e seen i nF ig ure 18.3, ur i cac id an d t h eot h er n i tro g enous waste p ro d uct s are d er i ve df rom two sources, nuc l e i cac id san dp rote i ns. De g ra d at i on o f nuc l e i cac id s is o f m i nor i mportance; most n i trogenous waste comes f rom prote i n b rea kd own f o ll owe d b y synthesis of hypoxanthine from amino acids. The biochemical reactions that lead t o s y nthesis of this p urine a pp ear to be similar to those found in other uric acid-excretin g or g an i sms (Burse ll ,19 6 7; Barrett an d Fr i en d , 1970) . 5 42 C HAPTER 18 T ABLE 1 8 .1. N itro g enous Excretor y Products of Various lnsect s a , b U ric acid Allantoin Allantoic acid U rea Ammonia Amino acid s Od onat a Aeshna c y ane a ( larva ) 0.08 — 0.00 —1 .00 — Dictyoptera/Phasmid a Perip l aneta americana 1 . 00 0 . 00 0 . 00 — — — Bl atta orienta l is 0.64 0.64 1.00 — — — Di x ipp us morosu s 0.6 9 1.00 0.44 — — — Hem i ptera Dy s d ercus f asciatu s 0.00 1.00 0.00 0.2 6 — 0.2 4 R hodnius p rolixu s 1.00 — — 0.33 — Trace Coleoptera M e l o l ont h avu lg ari s 1 . 00 0 . 00 0 . 00 — — — Attagenus piceu s 0.7 2 — — 1 .00 0.57 0.50 Dipter a L uci l ia sericata 1 . 00 0 . 30 — — 0 . 30 — L uci l ia sericata ( p u p a) 1.00 0.00 — — 0.1 5— L ucilia s ericata ( larva ) 0.05 0.0 2 ——1 .00 — L ep id opter a Pieris b rassica e 1 .00 0.04 0.01 — — — P ieri s bra ss ica e (p u p a) 1.00 0.03 0.0 5 —— — P ieri s bra ss ica e ( larva) 0.28 0.16 1.00 — — — a From Bursell ( 1967 ) , after various authors. b The q uantit y of nitro g en excreted in the different p roducts is ex p ressed as a p ro p ortion of the nitro g en in the p redominant end p roduct . F IGURE 18. 3. M eta b o li c i nterre l at i ons hi ps o f n i trogenous wastes. [A f ter E. Burse ll .19 6 7. T h e excret i on o f n i tro g en i n i nsects . A d v. Insect P hy sio l . 4 :33– 6 7. B yp erm i ss i on o f Aca d em i c Press Lt d .an d t h e aut h or.] 54 3 N ITR O GEN O U S EXCRETION A ND S ALT AND WA TER BALANC E I n addition to the enzymes for uric acid synthesis there are also uricolytic enzymes tha t catal y ze de g radation of this molecule in man y insects (Fi g ure 18.3). Uricase has a wide di str ib ut i on w i t hi nt h e Insecta. Act i ve p re p arat i ons o f a ll anto i nase h ave b een o b ta i ne df ro m m an y s p ec i es, b ut t h e di str ib ut i on o f t hi s enz y me a pp ears to b e rat h er restr i cte d com p are d wi t h ur i case. A l t h oug h t h ere are reports t h at i n di cate t h e occurrence o f a ll anto i case an d u rease in tissue extracts from a few insects, their presence should not be regarded as havin g b een established une q uivocall y . In other words, when urea and ammonia are p roduced i n s ig n i ficant amounts, t h e y are p ro b a bly d er i ve di n a manner ot h er t h an by t h e d e g ra d at i on of ur i cac id .T h eex i stence o f an orn i t hi ne c y c l e f or urea p ro d uct i on, suc h as i s f oun di n verte b rates, h as not b een prove d conc l us i ve l y, even t h oug h t h e const i tuent mo l ecu l es o f t h e cycle (arginine, ornithine, and citrulline) and the enzyme arginase have been identified in several species (Cochran, 1975). Cochran (1985) suggested that urea is merely a by-produc t of t h e bi oc h em i ca l convers i on o f ar gi n i ne to p ro li ne, use di n fligh t meta b o li sm (C h a p ter 14, Section 3.3.5). Similarl y , the wa y in which ammonia is p roduced (es p eciall y in those insects i nw hi c hi t i sama j or excretory mo l ecu l e) i s poor l yun d erstoo d .It i s genera ll y assume d to r esult from deamination of amino acids, but the precise way in which this occurs remains u nclear . I t has been su gg ested that the most p rimitive state was that in which the com p lete series of ur i co ly t i c enz y mes was p resent, an d ammon i a was t h e excretor y mater i a l .As i nsects b e- came more i n d epen d ent o f water, se l ect i on pressures l e d to l oss o f t h e term i na l enzymes an d production of more appropriate excretory molecules. This simple view should be regarde d w ith caution. Thus, in some caterpillars, diet can affect the nature of the nitrogenous waste . I n certain insects substantial q uantities of a p articular nitro g enous waste molecule are p ro- d uce d , y et t h ea pp ro p r i ate enz y me i nt h eur i co ly t i c p at h wa yh as not b een d emonstrate d , an d v i ce versa; t h at i s, t h ee ff ects o f ot h er meta b o li c p at h wa y sma y overr id et h eur i co ly t i c system. In many i nsects (espec i a ll yen d opterygotes) t h e pre d om i nant n i trogenous excretor y product changes during development. For example, in the mosquit o Ae d es aegypt i urea is t he p rinci p al nitro g enous waste in the (a q uatic) larvae, while uric acid becomes dominant i n p u p ae an d a d u l t f ema l es (von Dun g ern an d Br i e g e l , 2001). I n Pieri sb ra ss ica e ( Le pid o p tera) th ema j or excretor yp ro d uct i nt h e p u p aan d a d u l t i sur i cac id ; i nt h e l arva t hi s com p oun d const i tutes on l ya b out 20% o f t h en i trogenous waste, a ll anto i cac id b e i ng t h e pre d om i nan t e nd product (Table 18.1). Indeed, in some Lepidoptera, the ratio of uric acid to allantoin m ay fluctuate widely from day to day (Razet, 1961, cited from Bursell, 1967). Of great i nterest will be determination of factors that stimulate inhibition or activation (de g radation o rs y nt h es i s?) o f ur i co ly t i c enz y mes so t h at t h e most su i ta bl e f orm o f n i tro g enous waste i s pro d uce d un d erag i ven set o f con di t i ons. 3 .2. Physiology of Nitrogenous Excretion Ur i cac id i s p ro d uce di nt h e f at b o dy an d/ or Ma lpighi an tu b u l es (occas i ona lly t h e midg ut) an d re l ease di nto t h e h emo ly m ph .Howt h e highly i nso l u bl eur i cac id i s trans p orte d i n the hemolymph remains unclear though the most likely means seems to be as the sodium o r potassium salt, or in combination with specific carrier proteins (Cochran, 198 5 ). The uric acid is secreted into the lumen of the tubules as the sodium or p otassium salt, alon g wit h o t h er i ons, water, an d var i ous l ow-mo l ecu l ar-we igh tor g an i cmo l ecu l es. In a t ypi ca li nsect , f or exam pl e Di x ipp u s , secret i on occurs a l on g t h e ent i re l en g t h o f t h etu b u l e. No resor p t i o n of mater i a l sta k es p l ace across t h etu b u l ewa ll ,an d urate l eaves t h etu b u l e i nso l ut i on. In t h e r ectum resorption of water and sodium and potassium ions occurs, and the pH of the fluid 544 C HAPTER 18 F I G URE 18 . 4 . Movements of water, ions, and or g anic molecules in the excretor y s y stems of (A ) Di x ipp u s a n d ( B ) Rh o dniu s. [ After R. H. Stobbart and J. Shaw, 1974, Salt and water balance: Excretion, in : T he Physiology o f Insect a ,2n d e d ., Vo l . V (M. Roc k ste i n, e d .). B yp erm i ss i on o f Aca d em i c Press, Inc. an d t h e aut h ors.] decreases from 6.8–7. 5 to 3. 5 –4. 5 . The combined effect of water resorption and pH chang e is to cause massive precipitation of uric acid. Useful organic molecules such as amino acid s and sugars are also resorbed through the rectal wall. The Malpighian tubule-rectal wal l excretor y s y stem thus shows certain functional analo g ies with the vertebrate ne p hron. The excret i on o f ur i cac id in D ixippus i s summar i ze di nF ig ure 18.4A . In Rh o dniu s ,w h ose tu b u l es s h ow structura l diff erent i at i on a l on g t h e i r l en g t h ,t h e p ro - c ess o f excret i on i s b as i ca ll yt h e same as i n Di x ipp us . However, in R hod niu s o n l yt he d istal portion of the tubule is secretory and resorption of water and cations begins in the p roximal p art. Sli g ht chan g ein p H occurs (from 7.2 to 6.6) as the fluid p asses alon g 5 4 5 N ITR O GEN O U S EXCRETION A ND S ALT AND WA TER BALANC E t he tubule and this is sufficient to initiate uric acid precipitation. Further water and salt r esor p tion occurs in the rectum ( p H 6.0), causin gp reci p itation of the remainin g waste ( F ig ure 18.4B). A l t h ou gh a ll anto i n i st h ema j or n i tro g enous waste i n man yi nsects, i ts mo d eo f excret i on appears to h ave b een stu di e di non l y one spec i es, Dysdercus fasciatus ( Hem i ptera) (Berr id ge , 196 5 ). This insect is required, because of its diet, to excrete large quantities of unwanted i ons (ma g nesium, p otassium, and p hos p hate). This, combined with the insect’s inabilit y t o act i ve ly resor b water f rom t h e rectum, resu l ts i nt h e p ro d uct i on o f a l ar g evo l ume o f ur i ne. Because no resor p t i on or ac idi ficat i on occurs w hi c h cou ld cause p rec ipi tat i on o f ur i cac id, thi smo l ecu l e i sno l onger use d as an excretory pro d uct. T h us, a ll anto i n, w hi c hi s10t i mes m ore soluble than uric acid (yet of equally low toxicity), is preferred. However, the insec t d oes not possess a mechanism for actively transporting this molecule from the hemolymph t otu b u l e l umen; t h at i s, a ll anto i non ly moves p ass i ve ly across t h ewa ll o f t h etu b u l e. It is th ere f ore ma i nta i ne di n high concentrat i on i nt h e h emo ly m ph to ac hi eveasu f fic i ent rate o f diff us i on i nto t h etu b u l e. W h et h eras i m il ar mec h an i sm occurs i not h er a ll anto i n-excret i n g i nsects remains to be seen. It may be significant that many other allantoin producers are h erbivorous and have the problem of removing large quantities of unwanted ions. The p h y siolo g ical mechanisms for excretion of other nitro g enous wastes are p oorl y un - d erstoo d .A q uat i c i nsects are p resume d to excrete ammon i a i nver y dil ute ur i ne, w h ereas l ar - va eof m eat-eat i ng fli es suc h as Lucilia cu p rin a a n d S. bullata p ro d uce hi g hl y concentrate d , ammonia-rich excreta, apparently by actively transporting ammonium ions across the ante - r ior hindgut wall. Urea probably moves passively into the Malpighian tubules and becomes concentrated in the hind g ut because of its inabilit y to p ermeate the cuticular linin g as water r esor p t i on occurs. 3 .3. S torage Excretion An alternative strate gy to the removal of wastes throu g h the Mal p i g hian tubule-rectum s y stem use dby some i nsects i s stora g e excret i on, t h e retent i on o f t h e wastes i n “out o f t he way pl aces” w i t hi nt h e b o dy .InDysdercu s ,f or exam pl e, ur i cac id i s d e p os i te dp ermanent ly i nt h eep id erma l ce ll so f t h ea bd omen, f orm i ng di st i nct, w hi te transverse b an d s (Berr id ge, 196 5 ). Adult Lepidoptera convert much of their waste nitrogen into pteridines that are stored i n the integument, eyes, or wing scales, giving the insects their characteristic color pattern s ( Cha p ter 11, Section 4.3) . A tot h er t i mes stora g eo f urate occurs even w h en t h etu b u l es are wor ki n g norma lly a n d may b e regar d e d as a supp l ementary excretory mec h an i sm f or occas i ons w h en t he t ubules cannot cope with all the waste that is being produced. In the larval stages of many species uric acid crystallizes out in ordinary fat body cells and epidermis, even though the Mal p i g hian tubules are functional. It a pp ears that this is caused b y the metabolic activit y o f t h ece ll st h emse l ves ( i .e., t h e y are not accumu l at i n g ur i cac id f rom t h e h emo ly m ph ) , a n d cr y sta lli zat i on occurs by v i rtue o f t h e p art i cu l ar con di t i ons ( p H, i on i c content, etc.) e xisting in the cells. During the later stages of pupation the crystals disappear, the uri c a cid apparently having been transferred to the meconium (the collective wastes of pupal m etabolism, released at eclosion) via the excretor y s y stem. It is worth notin g that in man y s p ec i es t h eMa lpighi an tu b u l es are ent i re ly reconst i tute dd ur i n g t h e p u p a l sta g e. T h us, stora g eo f ur i cac id i n f at b o dy an d e pid erma l ce ll s i so fg reat i m p ortance at t hi st i me. Ye t ot h er i nsects, nota bl y term i tes an d coc k roac h es, reta i n l arge quant i t i es o f ur i cac id i n spec i a l cells (urocytes) within the fat body. However, as Cochran (198 5 ) pointed out, this is not a 5 4 6 C HAPTER 18 f orm of storage excretion but an important means of conserving nitrogen in these insects w hose normal diet is severel y nitro g en deficient (Cha p ter 16, Section 5.1.1). T em p orar y stora g eo f ot h er mater i a l sma y a l so ta k e pl ace. Ca l c i um sa l ts (es p ec i a lly c ar b onate an d oxa l ate) are f oun di nt h e f at b o d yo f many p l ant-eat i ng i nsect l arvae. Dur i n g metamorphosis they are released and dissolved, to be excreted via the Malpighian tubules in the adult. Dyes present in food are often accumulated in fat body cells where they appear to become associated with p articular p roteins. These p roteins are then transferred to the e gg d ur i n g v i te ll o g enes i san d t h e dy es su b se q uent ly “excrete d ” d ur i n g ov ip os i t i on. N e ph roc y tes (C h a p ter 17, Sect i on 2) accumu l ate a var i et y o f su b stances, es p ec i a lly p igments, and their name is derived from the mistaken idea that storage excretion is one o f their major functions. As Locke and Russell (1998) pointed out, nephrocytes are involved in the metabolism of hemol y m p h macromolecules . 4 . S alt and Water Balanc e Salt and water balance involves more than sim p l y the control of hemol y m p h osmotic p ressure; t h ere l at i ve p ro p ort i ons o f t h e i ons t h at contr ib ute to t hi s p ressure must b ema i n- ta i ne d w i t hi n narrow li m i ts. T h e osmot i c p ressure o f t h e h emo ly m ph i s g enera lly w i t hi n t h e same li m i ts as t h at o f t h e bl oo d o f ot h er organ i sms, b ut i t can b e i ncrease d cons id era bly under specific conditions (by the addition, for example, of glycerol, which serves as an antifreeze durin g hibernation). Re g ulation of the salt and water content is obviousl y related to t h e nature o f t h e externa l env i ronment . Insects i n diff erent h a bi tats f ace diff erent osmot ic p ro bl ems. Nevert h e l ess, t h ese p ro bl ems h ave b een so l ve d us i n g t h e same b as i c mec h an i sm , name l y, t h e pro d uct i on o f a “pr i mary excretory fl u id ” i nt h eMa l p i g hi an tu b u l es f o ll owe d by differential resorption from or secretion into this fluid when it reaches the rectum. Fo r c larity the problems of insects living on land, in fresh water, or in brackish or salt water are c ons id ere d se p arate ly . However, cons id era bl es i m il ar i t yi nt h eso l ut i on o f t h ese p ro bl ems will b e seen . 4. 1 . Terrestr i al Insects T errestrial insects a pp ear able to re g ulate their hemol y m p h osmotic p ressure over a wid e ran g eo f con di t i ons. For exam pl e, in T ene b ri o t h e h emo ly m ph osmot i c p ressure var i es o nly from 223 to 36 5 mM/l (measured as the equivalent of a sodium chloride solution ) o v e ra r ange of relative humidity from 0% to 100% (Marcuzzi, 19 5 6, cited in Stobbart and S haw, 1974). In starvin g S c h istocerc a there is only a 30% difference in hemolymph osmotic p ressure between animals ke p t in air at 100% relative humidit y and g iven onl y ta p water an d t h ose k e p t i na i r at 70% re l at i ve h um idi t y an dgi ven sa li ne (osmot i c p ressure e q u i va l ent to 5 00 mM/l sodium chloride) to drink (Philli p s, 1964a) . In terrestrial insects water is lost (1) by evaporation across the integument, although this is considerably reduced by the presence of the wax layer in the epicuticle (Chapter 11 , S ection 2); (2) durin g res p iration throu g h the s p iracles [man y insects p ossess devices both p h y siolo g ical and structural for reducin g the loss (Cha p ter 15, Section 2.2)]; and (3) durin g excret i on. Des pi te t h ese a d a p tat i ons, i nsects t h at i n h a bi t extreme ly d r y env i ronments ma y become greatly dehydrated. For example, some desert beetles can survive the loss of 7 5% o f their body water. The critical factor for these beetles is to maintain the intracellular w ater concentration b y usin g the water in the hemol y m p h; in other words, the hemol y m p h [...]... EXCRETION AND SALT AND WATER BALANCE TABLE 18. 2 The Osmotic Pressure and Concentration (mM/l) of Some Ions in the Hemolymph (H), Malpighian Tubule Fluid (MT), and Rectal Fluid (R) in Insects from Different Habitatsa 548 CHAPTER 18 Ions Fluid Osmotic pressure (≡NaCl solution) Na+ K+ Cl− Habitat Species (stage and conditions) Terrestrial Schistocerca gregaria (adult, water-fed) H MT R 214 226 433 108 20 1 11... studied In mosquito larvae a pair of papillae is located on each side of the anus (Figure 18. 7A) They communicate with the hemocoel and are well supplied with tracheae Their walls are a one-cell-thick syncytium (perhaps an adaptation to eliminate intercellular leakage) and covered with a thin cuticle (Figure 18. 7B) Mosquito larvae can accumulate chloride, sodium, potassium, and phosphate ions against... Brackish-Water and Saltwater Insects Brackish water may be defined as water whose osmotic concentration is in the range 300 mOsm (about 1.1% sodium chloride) (the osmotic concentration of the hemolymph) to 1000 mOsm (about 3.5% sodium chloride) (the concentration of normal seawater), with salt water having osmotic concentrations greater than those of natural seawater The definitions 552 CHAPTER 18 FIGURE 18. 7... those of sodium 554 CHAPTER 18 FIGURE 18. 9 Excretory system of saltwater mosquito larvae Known pathways of active ion transport are shown AR, anterior rectal segment; MG, midgut; MT, Malpighian tubule; PR, posterior rectal segment [After T J Bradley, 1987, Physiology of osmoregulation in mosquitoes, Annu Rev Entomol 32:439–462 Reproduced, with permission, from the Annual Review of Entomology, Volume... author.] 549 NITROGENOUS EXCRETION AND SALT AND WATER BALANCE 550 CHAPTER 18 against a concentration gradient and independently of the movement of water Furthermore, the rate of accumulation of these ions depends on their concentrations in the rectal fluid and the hemolymph In this way the requirements of the insect can be satisfied In water-fed locusts ions are resorbed from the rectum as quickly as they... and ionic content over a wide range of external concentrations (Figure 18. 8) In contrast to saltwater forms, brackish-water insects become osmoconformers in external media more concentrated than their hemolymph; that is, their hemolymph osmotic pressure increases approximately parallel with that of the surrounding medium (Figure 18. 8) Unlike the situation in freshwater species, however, where osmoconformation... Schistocerca gregaria (adult, water-fed) H MT R 214 226 433 108 20 1 11 139 22 115 93 5 Dixippus morosus (adult, feeding) H MT R 171 171 390 11 5 18 18 145 327 87 65 — Rhodnius prolixus (adult, 19–29 hr after meal) H MT R 206 228 358 174 114 161 7 104 191 155 180 — Aedes detritus (larvae, in seawater) H MT R 157 — 537 — — — — — — — — — Aedes detritus (larvae, in distilled water) H MT R 97 — 56 — — — —... tubule However, the fine-structural and experimental study of Grimstone et al (1968) has shown this conclusion to be wrong These authors found that the leptophragma cells have a normal complement of mitochondria Active transport of potassium ions occurs across the cells, which are, however, impermeable to water Chloride ions follow passively The scheme is summarized in Figure 18. 2D 4.2 Freshwater Insects... concentrations (Figure 18. 8) Larvae of Aedes detritus and Ephydra riparia, inhabitants of salt marshes, can survive in media containing the equivalent of 0 to about 7–8% sodium chloride Over this range of concentrations the hemolymph osmotic pressure changes by only 40–60% When their external medium is dilute (i.e., its osmotic pressure is less than that of the hemolymph), both brackish-water and saltwater... hemolymph), both brackish-water and saltwater insects osmoregulate to keep their 553 NITROGENOUS EXCRETION AND SALT AND WATER BALANCE FIGURE 18. 8 The relationship between osmotic pressure of the hemolymph and that of the external medium in some saltwater (sw) and brackish-water (bw) larvae [After J Shaw and R H Stobbart, 1963, Osmotic and ionic regulation in insects, Adv Insect Physiol 1:315–399 By permission . w h ereas l ar - va eof m eat-eat i ng fli es suc h as Lucilia cu p rin a a n d S. bullata p ro d uce hi g hl y concentrate d , ammonia-rich excreta, apparently by actively transporting ammonium ions across the ante - r ior. of uric acid, neither the nature of the factor(s) involved nor the site of action is k nown. Changes in the rate of uric acid production, for example, occur at speci c stages in an insect’s life. The combined effect of water resorption and pH chang e is to cause massive precipitation of uric acid. Useful organic molecules such as amino acid s and sugars are also resorbed through the rectal