Thoughts on Aquatic Insects

G. Evelyn Hutchinson

Aquatic adults seldom have terrestrialjuveniles. Respiratoryproblems may lead to the first one or two nymphal instars of tropical species being smaller than related temperate ones. Suctorial feeding on many aquatic insects such as the may- higher plants seems unknown. Cryptic coloration is common, aposematic, and epi- flies, the Hemiptera, and the aquatic rare. is but gamic Flightlessness common, potentially flying forms must be general- moth Acentropus, though later these de- ly available;this restricts tracheal gills to juveniles. 12 (Accepted for publication velop other respiratory mechanisms. January 1981) The unique pair of genera, Idiocoris and Paskia, the smallest of all known aquatic KINDS OF LIFE HISTORY ly rare, being exemplified only by certain Hemiptera, are apparently the only free- beetles of the families Hydraenidae and living adult apneustic insects; they are Among the insects of inland waters Dryopidae (Hinton 1955). Moreover, limited to the stony littoral of Lake Tan- there are certain peculiar situations though the aquatic bugs and beetles to- ganyika (Esaki and China 1927). which, though often obvious, at first gether include almost all the members of The large aquatic insects breathe ei- seem hard to explain. the adult aquatic and immature aquatic ther by tracheal gills, outgrowths of the We may group the animals under con- categories, the two orders differ in their body wall that are richly supplied with sideration according to whether they are relation to water: The endopterygote Co- trachea, or spiracles that may be fed terrestrial or aquatic in active immature leoptera have a pupa that is nearly al- from bubbles and replaced periodically and predominantly trophic stages or in ways formally terrestrial. It lies in a dry by visits to the surface or to photosyn- the mature and primarily reproductive cocoon in a cavity excavated above wa- thesizing plants. Such bubbles or air- climax of their lives. The following ma- ter-level in the bank of the water; the stores are held in various ways. Imma- trix shows the orders of magnitude of the larva lived in it, and all being well, the ture insects retain air-stores usually in four possible classes: adult may return to it. bunches of hair; in mature insects, the elytra of beetles or the hemel- Adult Adult equivalent ytra of bugs cover a large dorsal air- terrestrial aquatic RESPIRATION IN AQUATIC HABITATS store. There may also be very fine hairs air on the surfaces of various Immature carrying For a member of a terrestrial group parts of the body, which give the insect terrestrial n. 105 n. 102 entering freshwater, respiration proba- its "silvery-light" appearance, as Mary Immature bly poses a greater problem than does Ball (Ball 1846) called it 140 years ago. aquatic n. 104 n. 103 any other vital function. Small aquatic From the air-stores, air is usually passed insects (and other animals less than into the tracheal system much as in ter- about 1 mm in diameter) are apt to restrial insects. breathe by diffusion over the entire thin, Since the air in the air-store is in This reveals the fact that it is easier to be but largely unmodified, body wall. There contact with water, it can act as a immature in the water than to be mature. "phys- may be specialized hemolymph sinuses ical gill"-a universal, though rather The category of the aquatic mature stage below this wall. When the insect is a odd, appellation (Ege 1915, Popham that has grown up terrestrially is curious- relatively long and thin cylinder, one 1964, Thorpe 1950). As respiration takes may regard the whole body as a gill. place, oxygen is removed; the equivalent Hutchinson is Sterling Professor of Zoology (emeri- tus) and senior research biologist, Department of Many variations on this general theme carbon dioxide produced is much more Biology, Yale University, New Haven, CT 06511. are found in the Diptera, which common- soluble than the oxygen and quickly This paper is derived from a lecture given on 12 ly have blood gills or special diverticula into the so that the bubble September 1980 to Ruth Patrick's course on the passes water, biology of streams, School of Forestry and Environ- of the body wall containing sinuses. In constituting the air-store contracts. The mental Studies, Yale University. He is greatly in- many cases, however, these have now partial pressure of nitrogen in the bubble debted to her and to the school for giving him the been shown to be opportunity to present this material, which is based organs taking up chlo- therefore increases, so nitrogen diffuses on a far more extended treatment (with a much fuller ride ions rather than oxygen. In some out. Since oxygen is lost by respiration, set of references) to appear in the fourth volume, on chironomids, the hemolymph contains the partial pressure of that gas de- zoobenthos, of his Treatise on Limnology. ? 1981 American Institute of Biological Sciences. All rights hemoglobin. Comparable respiration in- creases, and oxygen diffuses into the reserved. volving the whole surface is common in bubble, at least from saturated water.

July/August 1981 495 Ideally, the process can continue until The insects that have perfected this lova americana Desmoulins from the all the nitrogen has been lost; but in respiratory plastron live in habitats Lower Permian of Oklahoma. Because actual cases, as the bubble becomes where continualdisturbance, or the pho- the mandibleswere very large and bore small, the oxygen content becomes dan- tosynthetic activity of calcicole algae, teeth, Kukalova(1968) initiallyregarded gerously low, and the air-store must be keeps the water saturatedwith oxygen. the insect as a carnivore. Later, Hub- replaced at the surface, well before it Though in a perfectly developed case, bard and Kukalova-Peck (1979) com- disappears. The effectiveness of the such as that of Aphelocheirus, the plas- paredthe mouthparts with some modern process depends on the oxygen concen- tron obviates the necessity for surfacing, generalistfeeders. Though the evidence tration in the water, which is related it is evidently not a mechanismthat can is still inadequate,it seems that the may- inversely to the temperature.It also de- be effective in a wide variety of habitats. flies may exemplify a trend detectible in pends on the exposed surface of the A second specialization of the air- other freshwaterinvertebrates that have bubble, which, in a large animal, is store is found in the lesser backswim- evolved a kind of selective omnivory. smallerrelative to the mass of metaboliz- mers of the subfamilyAnisopinae in the For such animals,the haptobenthicalgae ing tissue than in a small one. Thus, the family Notonectidae:the generaAnisops and bacteria with the slime secreted by physicalgill works best for small animals living in the warmtemperate and tropical them, together with adherent detritus at low temperatures, but the effective- Old World and Buenoa in the New. and associated small animals, constitute ness varies greatly with the morphology These insects have an abdominalhemo- a universal pabulum covering all sur- and physiology of the organism under globinorgan, richly suppliedwith trache- faces, at least in the shallower parts of study. Under favorable circumstances, ae. The hemoglobinin the cytoplasm of temperate freshwaters (except perhaps the mechanism of the physical gill can the cells of the organ is charged with the most oligotrophic). A change from certainlyincrease severalfold the period oxygen at surfacingand slowly liberates carnivory to partial reliance on such a between surfacing,thereby reducingthe the gas as it is used in respiration.The source of food, together with any other risk of predation. insect thus can adjust its density, re- plant or animalmatter that may be avail- High temperaturesnot only decrease maining poised at the same depth for able, seems to characterizemany of the the physical gill's effectiveness, but also some minutes (Miller 1964). small Corixidae and some species of increase the metabolic demand for oxy- Most adultinsects living on the bottom Haliplidae. gen. Very little, unfortunately,is known or among weeds, if they use an air-store Development of a like kind of omniv- about respirationin tropical aquatic in- for respiration, will have to make fre- ory is known in the Lymnaeidae among sects, thoughMiller (1964)has clear evi- quent visits to the surface, except per- the watersnails. In all cases, some de- dence that the physical gill can work for haps when dormantin winter. Such ex- gree of selectivity is retained,though the Enithares sobria Stal, a backswimmer peditions are energetically wasteful and rangeover which it is exercised is greatly widespreadin CentralAfrica. In the Cor- limit the depths that can be colonized. extended. Some animals eat most algae ixidae, the largerCorixinae are predomi- Moreover, surfacing is bound to be a other than Cladophora, or most angio- nantly temperatewith a maximumnum- conspicuous act, increasing the dangers sperms other than Elodea. These two ber of species in the United States, of predation.In spite of these disadvan- plants are apparently largely inedible whereas the smaller Micronectinae are tages, no adult aquaticinsect respires by (and so most successful). The former is largely tropical with the richest local trachealgills, though such structuresare apparentlyprotected by lauric, myristic, fauna in Sri Lanka. In tropical uplands, obviously highly successful in the physi- and palmitoleic acids (Lalonde et al. such as the Nilgiri Hills in India and the ology of mayflyand stonefly nymphsand 1979, Larson 1981), which render the mountains of Ethiopia, Micronectinae, in more elaborateways in those of drag- plant poisonous, or at least inhibitoryin as in temperateregions, tend to be rarer onflies and damsel flies, in the larvae of variousways to mosquitolarvae, gastro- than Corixinae. These features of the alderfliesand caddisflies, and in those of pod mollusks, and crayfish.' Unfortu- distributionsof the Corixidae are, thus, some beetles and two-winged flies. nately, except for Nuphar and Nelumbo in line with small species being better (which are full of strangealkaloids), little adapted to warm climates, be- perhaps A TRENDTO SELECTIVEOMNIVORY is known of secondary compounds of a cause they have greater ease in defensive kind in freshwater vascular breathing. The feeding habits of aquatic insects plants. The existing data (or lack of it) Two remarkable respiratory special- are much more varied than their modes suggest that such compounds are of less izations are known in particulargroups of respiration. Usable energy and the significancethan on land, but this well of submergedinsects. A few species of elements required in nutrition, other may be an illusion based on ignorance. naucorid bugs and elminthid beetles than hydrogenand oxygen, are obtained Even the most inedible plant will ulti- have evolved an extreme developmentto from many sources in a variety of ways. mately add to the food reserves, produc- the physical gill. A large area of the body The earliest putative aquatic insects, ing, when it dies, detritus and nutrients is covered with a pile of very fine short the Protodonata,were presumablycarni- for algae and bacteria. hydrophobe hairs. In the Palaearctic vores, as are theirimmediate successors, Generally, almost any moving food naucorid Aphelocheirus, there may be the Odonata. The largest Protodonata, may be pursued by predatory aquatic 2.5 millionsuch hairs (about6ix long) per giants with a wingspan of up to 75 cm, insects, though the size and ease of han- mm2 (Thorpe 1950). At ordinary sub- must have had proportionately large dling make a great difference to what is aqueous pressures, surface forces pre- nymphs of great repacity, which proba- actuallytaken. There are very few cases vent water from penetrating the pile, bly took a number of years to reach of food being rejected: Notonecta undu- which remainsthe supportfor a thin dry maturity.In their late instars, they may gaseous layer, acting as a physical gill, well have eaten fishes. 'RuthPatrick, School of Forestryand Environmen- from which specialized spiracles can re- The oldest mayflynymph of which the tal Studies, Yale University, personal communica- ceive air. mouthparts are known in detail is Kuka- tion, November 1980.

496 BioScience Vol. 31 No. 7 lata Say refused a pink phyllopod of ately colored bottom, they leave. Both in In most Corixidae, the male bears on uncertain identity; N. uhleri Kirkaldy the laboratoryand in nature, the match- the right side of the sixth abdominal will not eat Buenoa; and a few of the ing can be shown to be effective against tergitea condensed groupof spines, usu- Belostomatidaeare specialized as preda- predation(Popham 1942, 1944). ally formingseveral regularrows, called tors on gastropodsnails. A similartendency to match a light or the strigil. In the very primitiveAustra- Most waterbugsare still suctorial car- dark backgroundoccurs in some water- lian Diaprepocoris, the strigil is double, nivores; this is probably true of many beetles, notably the Haliplidae.2Howev- as if the left member of a pair of lobes corixids, even though others feed on er, in holometabolous insects, which had moved across the body to engage haptobenthos. Indeed, fully aquatic in- may have differentlarval and adult habi- with the right, perhaps makinga sound- sects have not developed the habit of tats, the variationin the adults is proba- producingorgan. In the small and largely suckingthe fluid contents from vascular bly determined genetically rather than tropical Micronectinae,the strigil is de- waterplants, though corixids and some environmentally. veloped as a row of short, wide spines on larval haliplids may suck out all the Many beetles secrete toxic secondary the rightof the sixth abdominaltergite of contents of the cells of filamentousalgae. compounds in their pygidial or thoracic the male. It is certainly a sound-produc- Thereare no freshwateranalogues to the glands (Miller and Mumma 1976, ing organ, pluckedby a plectrumformed vast array of Myridae in the Heterop- Schildknecht1970). In the Dytiscidae, at from the right posterior margin of the tera, nor to the whole of the Homoptera. least in the subfamilies containing the fifth tergite (King 1976). In the latter suborder, a few aphids are largerspecies (Dytiscinae and Colymbe- In the Corixinae, a well-developed found on the aerial parts of emergent tinae), the thoracic glands produce an strigil is present in most species. Mary waterplants, but not under water. The astonishingarray of steroids relatedto or Ball (Ball 1846), who first heard Corixi- absence of aquatic insects that suck identicalwith mammaliansex hormones. dae stridulatein 1840, recorded abdomi- higher plants may be of great antiquity. These are repellent, anaesthetic, or, in nal movements, as in Micronecta, ac- The Paleoptera, the more primitive sufficient dosage, lethal to fish. In the companyingone type of sound made by group of flying insects, seems to have Gyrinidae,norsesquiterpenes, produced Sigara dorsalis (Leach). No one else has consisted in the late Palaeozoic of man- in the pygidialglands, act similarly.The seen any part other than the anteriorlegs dibulate orders with aquatic nymphs, other families of waterbeetles have not being moved in relationto sound produc- which survive as mayflies and dragon- been adequately studied, and the water- tion in the Corixinae. In this subfamily, flies, and extinct terrestrial haustorial bugs, as well as the beetles, produce the strigil is probably used to increase orders (Palaeodictyoptera, Megasecop- odors that may be repellent,but relative- the grip of the male on the female during tera, and Diaphanopterodea),the suck- ly little work has been done on their coitus, though in many cases the struc- ing mouthpartsof which are apparently chemistry. ture looks like a sound-producingorgan. derived from mayfly-like trophi (Hub- In the Corixinae,the known stridulatory bard and Kukalova-Peck Kuka- 1979, AND structuresare a patch of short, pointed lova-Peck BREEDING,ASYMMETRY, 1978). SONG spines forming a pars stridens on the anteriorfemur of the males of many and There are certain very peculiar spe- the females of a few species, and a cializationsrelated to CRYPTICCOLOR AND CHEMICAL reproduction.For plectrum,a ridge on the edge of the head the most DEFENSES part, they do not yet fit in with on which the pars stridens is rubbed the other aspects of the life of insects (Jansson 1972). The sounds are mainly Aquatic insects are, of course, them- underwater to make a unified story. used in courtship, but they also may be selves subjectto predation.Macan (1966) Hungerford (1919) indicates that the employed to achieve a certain degree of particularlyhas shown how importantthe male of Notonecta irrorata Uhler habit- spacing between males in a sort of terri- littoralvegetation can be in determiningif ually takes up a position to the left of the torialarrangement. Very remarkabledif- such insects can coexist with fish. The female in mating, even though his exo- ferences in behavioron the part of close- matter is clearly very complicated, de- skeleton and genitaliaare not asymmetri- ly allied species have been recorded by pendinglargely on the species of predator cal. In some naucorids,notably the com- Jannson (1979); the comportmentof the and prey as well as the nature of the mon European Ilyocoris cimicoides male of Arctocorisa germari (Fieber), protectiveenvironment. (Linnaeus), the muscles of the male ab- which always waits for a reply from the Striking reactions to predation have domen are asymmetrical, even though female he is courting, contrasts with the evolved. Popham(1941) found that most the exoskeleton is not. In some tropical activity of A. carinata (Sahlberg),which corixidstend to matchthe albedo of their members of the family (Macrocoris, often engages in rape (Jansson 1979). background.The process is ontogenetic, Neomacrocoris), the seventh tergite of Though in most genera the strigil lies dependingon the backgroundto which the male has asymmetricallobes on its on the right side of the sixth abdominal the insect is exposed three days before a posterior margin, but their function is tergite, throughoutthe family occasional moult. The corixids are so imprintedon unknown. The Anisopinae have asym- sinistral specimens are recorded in a the backgroundthat they become rest- metrical parameres or claspers, though numberof species. A few are regularly less when placed on one that they do not the rest of the abdominalbodywall ap- dimorphic, and others (Corixa, Tricho- match, even though they probablyhave pears symmetrical.In the Corixidae,the corixa, Heliocorisa) practically always no way-because of the geometry of whole of the abdominal exoskeleton have the strigil on the left. When this theireyes and dorsal surfaces-of direct- from the fifth tergite backwards is ex- inversionoccurs, it affects only the mus- ly comparingtheir own coloration with tremely asymmetrical. cles and exoskeleton of the abdomen; that of the backgroundon which they are other asymmetriesremain unchanged. In perching.If, after a migratoryflight, they one of the dimorphicspecies, Ahuautlea enter a body of water with an inappropri- 2E. J. Pearce, personalcommunication. mexicana de la Llave, the homozygous

July/August 1981 497 sinistral is lethal (Peters 1960). (There existence of the rare flying forms is im- textures have tracheal gills. Why, when must be intense selection of heterozy- portant in dispersal (Wr6blewski 1958). such organs would seem advantageous, gotes bearingthe sinistralgene.) In Micronecta in tropical lands, many do no adults? Perhaps, if an insect is to Very elaborate sound-producing species are always-and most are fre- have gills, it must either give up flightor mechanisms used in courtship are also quently-winged, suggesting that in ar- develop some mechanism for keeping found in the small backswimmersof the eas in which shallow water frequently the gills moist on land and in the air. subfamily Anisopinae: Anisops in the dries up, flight is an essential function. Land crabs can do this, walkingeven on Old World,Buenoa in the New. The few Flightless Corixidaewith undeveloped dry coral islands, as the branchialcavity of the 175 species that have been studied muscles live longer and are more fertile provides a way to keep the gills moist. differ markedly in the details of their under suboptimal,but not under optimal But there is no obvious preadaptation behavior. The Anisopinae use a tibial conditions, than fully developed speci- that would permit the development of comb on the anteriorleg againsta pair of mens. When conditions are poor, the such a shield in either order containing prong projections for the beak as their economy of not having to support the adult aquatic insects. Though many spe- main vocal organs; as well as sound, a basal metabolismof a thoraxfull of flight cies of aquatic insects do not fly, very characteristicpattern of movementvary- musculatureevidently better adapts the little genetic or environmental change ing from species to species is involved in flightless forms, except that they are would probably be needed to convert courtship(Goertz 1963, Wilcox 1975). unable to fly away (Young 1965). almost any actual nonflyingspecies into Sound productionis also recordedbut Less is known about the pterygo- one that can fly. Whatever may cause hardly studied in a few other waterbugs dimorphism of beetles (Jackson 1956) the appearanceof fully developed mac- and waterbeetles. Where it is used in an than of bugs, but there is some evidence ropterousforms in up to about 2%of the elaborate way in courtship, as in the that the condition is genetic (Angus populationof the Palaearctic species of Corixidaeand Anisopinae,it seems char- 1970). Micronecta,the chance of any individual acteristic of rather gregarious species being able to fly is small. But the chance ordinarily exhibiting little of there intraspecific THE DANGERSOF BEINGTOO being some individuals, in a unlike the canni- aggression, potentially AQUATIC drying habitat, that could fly away to a balistic and very well-spaced Notonec- more permanentbody of water is great. tini. This needs further study, as does In transient environments, which Wr6blewski(1958) has given actual ex- the possibility that underwaterauditory nearlyall bodies of freshwaterultimately amples that indicate that such behavior stimuli are better epigamic signals than are, some opportunity for dispersal is would be quite possible in nature. In an are visual ones. Of course, they may be necessary for the continued existence of extreme case of genetically determined dangerousif there are predatorsaround a species. The nearerthat this opportuni- wing development, back-mutationmight with receptor organs for sound. As in ty is to the reproductivephase in the life be successfully balanced against the se- fishes (Popperand Coombes 1980),pitch history, the more effective it will be. For lection in favor of a flightlessform. This plays little or no part in communication, any generation, the population will be would permit survival of the species so which is primarilybased on the length greatestwhen present as newly fertilized long as aerialrespiration remained possi- and spacing of trains of pulses. eggs before any mortality has occurred ble. If tracheal gills had been evolved, and with the maximalchance of at least a the species might be completely unable FLIGHTAND FLIGHTLESSNESS few individuals being delivered into to look for new habitats as the water some unusually favorable environment. dried up. Thus, the only adult aquatic Finally, there is a systematic differ- Since, to a flying insect, the period of insects without open spiracles are the ence between the flightless forms of ter- flight is also the period of maximum minute Idiocoris and Paskia, which live restrialbugs, usually apterouswith vesti- potential dispersal, aeroterrestrial life in one of the two lakes that are least gial elytra, and the flightless waterbugs would be expected at the time of repro- likely to have dried out completely for and waterbeetles,in which the hemelytra duction. This would explain the rarityof many millions of years. or elytra are almost always large enough species with terrestriallarvae and aquat- Throughoutthe Mesozoic, the rise of to cover a significant dorsal air-store. ic adults. the angiospermsmust have permittedthe Only when there is a respiratory plas- The absence of any adult insects with developmentof a modernmarginal flora, tron, as in Aphelocheirus, does a condi- tracheal gills at first seems peculiar be- which provides protectionagainst exces- tion develop comparable to what is cause any kind of respiration involving sive predationby fish and a place where found on land. surfacingis always wasteful and necessi- insect predators may lurk unseen while Very often in those Corixinaein which tates the use of energy in moving to or waiting for the appearanceof their own neitherhemelytra nor wings are reduced, fromfeeding groundsto the surface. The prey. The early immatureaquatic insects the insect is flightless because the indi- range of depths that can be occupied is seem to have had gill-plates,producing a rect flight muscles that normallyfill the clearly limited; nearly all waterbugsand simple current used in dermal respira- thorax fail to develop at the last moult waterbeetlesnever descend below a few tion. Kukalova-Peck (1978), reviewing (Young 1965). This failure is usually meters. Moreover, surfacingis a danger- the many theories put forward as to the temperature-dependent;only over about ous activity not only to insects in torren- origin of the insect wing, makes a clear 15? C does the adult insect emerge as a tial waters for mechanical reasons, as case for regarding wings and the gill- flying form (Scudder 1976, Scudder and Parsons (1974) has pointed out, but also plates of Ephemeropteraas serially ho- Meredith1972). In the Micronectinaeof because, by making insects move con- mologous, e.g., in an organism such as temperate countries, nearly all speci- spicuously, it makes them more avail- the Permian mayfly nymph, Kukalova mens are flightless, about 2% having able to predators. americana (Kukalova 1968). She is, fully developed wings. The natureof the An enormous numberof immaturein- however, wary about attributing an determinationis unknown, though the sects of all sorts of shapes, sizes, and aquatic habitat to the ancestor of all the

498 BioScience Vol. 31 No. 7 Pterygota. The earliest such ancestor some islands in the western Pacific are Except among fishes, there is no cer- presumably continued to moult through- the most brilliant, but they are of rela- tain development of epigamic coloration out life without any sharp break in form tively recent marine origin. Some leech- in freshwater animals. The backswim- at a particular metamorphic moult. es and some mayfly nymphs have charm- mers of the western American subgenus There are several hypotheses as to the ing color patterns, but they are relatively Erythronecta show some sexual dimor- value of a series of lobes arising from the subdued. Among mollusks the most dec- phism in the color of their hemelytra, the first thoracic segment nearly to the end orative are certain Neritidae, notably in black and red females being the most of the abdomen, some not involving an the genus Theodoxus, which, like their brilliant of all aquatic insects. Though aquatic stage. However, the develop- marine allies, have porphyrin pigments there is evidence that in Notonecta un- ment of a clear-cut metamorphic moult in the shells (Comfort 1950). dulata males find their mates by sight at which the lobes on the second and The only reasonably clear cases of (Clark 1928) and that part of the com- third thoracic segments become func- aposematic coloring are provided by the pound eye of N. glauca Linnaeus is tional wings is consistent with a change scarlet water mites, which can be unpal- sensitive to differences in color (Rokohl of environment from water to air, as in atable (Elton 1922, Popham 1948).3 Ellis 1942), it is by no means certain that red the penultimate moult of a mayfly. So and Borden (1970) found that blood and black hemelytra, seen from below there may be an evolutionary connection worms were the least preferred kind of against the sky and obscured by a silvery here. food in a considerable selection offered air-store, would provide a very powerful From the serial homology so obvious to Notonecta undulata, suggesting that sexual stimulus. Except in the largest in the Kukalova nymph, we may reason- chironomid larvae, having acquired he- and clearest lakes, in which most of the ably expect at least the first aquatic moglobin for respiration, have evolved more spectacular freshwater fishes hav- insects to have had gill-plates, if not some impalatability as an appropriate ing epigamic colors are found, the water tracheal gills. As the phanerogamic litto- counterpoise to their increased conspic- may have always had just sufficient ral vegetation developed, underwater uousness when discovered by a predator brown organic stain to dull the kind of bugs or Nepomorpha (Popov 1971)-and nosing about on a shallow bottom. brilliance associated with mating behav- doubtless some of the families of water- The very striking series of poisonous ior on land. beetles-evolved. A second kind of secondary compounds in the Dytiscidae None of these explanations is proba- aquatic respiration with an airstore per- and Gyrinidae go unadvertised, doubt- bly adequate by itself to account for the mitted adults as well as nymphs or larvae less because the advantages of warning chromatic characteristics of the freshwa- to live underwater, and such insects coloration are more than offset by the ter fauna. Taken together, they doubt- were clearly prone to occupy some of the disadvantage a predator has in being less provide, in some cases, a partial new niches offered by a rich marginal conspicuous. However, at the surface a explanation. Certainly, our knowledge zone of angiosperms. The extensive hap- scintillating school of whirlgig beetles of aquatic insects is still not great tobenthos associated with these plants may be conspicuous enough to discour- enough to enable us to think about them would be a convenient source of food, age experienced predators such as birds. satisfactorily. perhaps better than the plants them- On land a large number of distasteful selves. The late appearance of the dia- species owe their unpalatability to sec- ACKNOWLEDGMENTS toms suggests that the haptobenthos, ondary compounds derived from their I wish to the of which must have existed as a layer of food plants. Such herbivorous species acknowledge help c.olorless and blue-green bacteria far into can safely develop warning coloration. three friends: Ruth Patrick has given me numerous and valuable of infor- the Precambrian, underwent consider- In freshwater the apparent rarity of pieces Charles L. has able further evolution throughout the Pa- plants containing such compounds mation; Remington put his enormous store of laeozoic. The development of a commu- would probably rule out this particular entomological at and nity capable of supporting a fairly rich strategy. It would be interesting to know learning my disposal; Nancy Knowlton has been a microfauna would have added to the whether the species of Donacia feeding lively ecological me from a serious error in nutrient value of the so-called universal on Nympheaceae sequester alkaloids critic, saving discussion of underwater coloration. freshwater pabulum. from their food plants, as the beaver my feeding on the same plants appears to do. There may be further reasons for the REFERENCES CITED drabness of most freshwater animals. In THE DINGINESS OF Angus, R. B. 1970. Genetic experiments on is to FRESHWATER INVERTEBRATES quiet water, eddy diffusivity likely Helophorus F. (Coleoptera, Hydrophili- be lower than in air, so that a repulsive dae). Trans. R. Entomol. Soc. Lond. 122: One further aspect of this story seems odor may be as effective a localized and 257-276. ripe for investigation. Freshwater ani- permanent warning as a bright color, Ball, R. 1846. [All but introductoryparagraph mals are notoriously dingy in color, as except perhaps for very small mobile is by Mary Ball, though she is not men- E. M. da Costa (1776), noticed more animals, such as watermites. The work tioned by name] Corixa striata, Curtis. than 200 years ago. One of the brightest of Popham (1948) suggests that poor col- Ann. Mag. Nat. Hist. 17: 135-136. colors found in limnetic animals is the or vision and poor learning capacity may Clark, L. B. 1928. Seasonal distributionand life of Notonecta undulata in the brilliant red of some planktonic cope- also play a part. Most aposematic color- history Canada. 9: 383- which Hairston has shown ation on land is Winnipegregion, Ecology pods, (1976) directed against birds 403. has with a purely physiological function, pro- superior color vision and adequate Comfort,A. 1950. Biochemistryof molluscan viding protection against excessive learning capacity. shell pigments. Proc. Malacol. Soc. Lond. short-wave solar radiation. Among larg- 27: 79-85. er invertebrates, a crimson polyclad in da Costa, E. M. 1776. Elements of Concholo- Borneo and a green opisthobranch on 3C. Kerfoot, personalcommunication. gy. B. White, London.

July/August 1981 499 Ege, R. 1915. On the respiratoryfunction of Jackson, D. J. 1956.The capacity for flightof Miller,J. R., and R. 0. Mumma. 1976. Phys- the air store carried by some aquatic in- certainwaterbeetles and its bearingon their iological activity of water beetle defensive sects. Zeit. Allg. Physiol. 17: 81-124. origin in the western Scottish Isles. Proc. agents. I. Toxicity and anaestheticactivity Ellis, R. A., and J. H. Borden. 1970. Preda- Linn. Soc. Lond. 167: 76-96. of steroids and norsesquitespenesadminis- tion by Notonecta undulata (Heteroptera: Jansson, A. 1972. Mechanismsof sound pro- tered in solutionto the minnowPimephales Notonectidae)on larvae of the yellow fever duction and morphologyof the stridulatory promelas Raf. J. Chem. Ecol. 21: 115-130. mosquito. Ann. Entomol. Soc. Am. 63: apparatusin the genus Cenocorixa(Hemip- Miller, P. L. 1964. The possible role of hae- 963-973. tera, Corixidae). Ann. Zool. Fennici 9: 120- moglobin in Anisops and Buenoa (Hemip- Elton, C. 1922.On the colours of water-mites. 129. tera: Notonectidae). Proc. R. Entomol. Proc. Zool. Soc. Lond. 1922(2): 1231-1239. . 1979. Reproductiveisolation and ex- Soc. Lond. 39 A: 166-175. Esaki, T., and W. E. China. 1927. A new perimental hybridization between Arcto- Parsons, M. C. 1974. Anterior displacement family of aquatic Hemiptera. Trans. Ento- corisa carinata and A. germani (Heterop- of metathoracicspiracle and lateral inter- mol. Soc. Lond. 1927(11): 279-295. tera, Corixidae). Ann. Zool. Fennici 16: 89- segmental boundary in the pterothoraxof Goertz, M. E. 1963. Sound productionin two 104. Hydrocorisa (Aquatic Hemiptera). Zeit. sympatric species of aquatic Hemiptera King, J. M. 1976. Underwatersound produc- Morph. Tiere 79: 165-198. Buenoa macrotibialis Hungerford and tion in Micronecta batilla Hale (Hemiptera: Peters, W. 1960. Inheritanceof asymmetryin Buenoa confusa. UnpublishedM.A. thesis, Corixidae). J. Austral. Entomol. Soc. 15: a water-boatman (Krizousacorixa femor- DartmouthCollege, Hanover, NH. 35-43. ata). Nature (Lond.) 186: 737. Hairston,N. G. 1976. Photoprotectionby ca- Kukalov,, J. 1968. Permianmayfly nymphs. Popham, E. J. 1941. The variation in the rotenoid pigments in the copepod Diapto- Psyche 75: 310-327. colour of certain species of Arctocorisa mus nevadensis. Proc. Natl. Acad. Sci. Kukalov,-Peck,J. 1978. Originand evolution (Hemiptera,Corixidae) and its significance. USA 73: 971-974. of insect wings and their relation to meta- Proc. Zool. Soc. Lond. Ser. A 111: 135- Hinton, H. E. 1955. On the respiratoryadap- morphosis, as documented by the fossil 172. tations, biology, and taxonomy of the Pse- record. J. Morphol. 156: 53-126. . 1942. Furtherexperimental studies of phenidaewith notes on some related fam- Lalonde, R. T., C. D. Morris, C. F. Wong, the selective action of predators. Proc. ilies (Coleoptera). Proc. Zool. Soc. Lon. L. C. Gardiner,D. J. Eckert, D. B. King, Zool. Soc. Lond. Ser. A 111: 105-117. 125:543-568. and R. H. Zimmerman.1979. Response of . 1944. A study of the changes in an Hubbard, M. D., and J. Kukalov,-Peck. Aedes seriatus larvae to fatty acids of C!a- aquatic insect population, using minnows 1979. Permian mayfly nymphs: new taxa dophora. J. Chem. Ecol. 5: 371-381. as predators. Proc. Zool. Soc. Lond. 114: and systematic characters. Pages 19-31 in Larson, R. 1981. Potentialfor biologicalcon- 74-81. J. F. Flannagenand K. E. Marshall, eds. trols of Cladophora glomterata. In a report . 1948. Experimental studies of the Advances in Ephemeroptera Biology. Plen- of the EnvironmentalProtection Agency. biological significance of noncryptic pig- um Press, New York. EPA, Washington,DC, in press. mentationwith special referenceto insects. Hungerford,H. B. 1919. Biology and ecology Macan,T. T. 1966.The influenceof predation Proc. Zool. Soc. Lond. 117: 768-783. of aquatic and semiaquatic Hemiptera. on the faunaof a moorlandfish pond. Arch. . 1964. The migrationof aquatic bugs Kansas Univ. Sci. Bull. 11 (21): 1-256. Hydrobiol. 61: 432-452. with special referenceto the Corixidae(He- miptera: Heteroptera). Arch. Hydrobiol. 60: 450-496. Popov, I. A. 1971. Istoricheskoerazvitie po- How To Gain Control Of Your luzhestkokrylykh infraotriada Nepomor- pha. Akad. Nauk. USSR., TrudyPalaeont. EnvironmentalControl Problems: Inst. 120, (in Russian). Popper, A. N., and S. Coombs, 1980. Audi- fishes. Am. Sci. CallSherer. tory mechanismsin teleost Ill _. 68: 429-440. Our and engineers designers Rokohl,R. 1942.Uber die regionaleVerschie- can help you select the optimum denhiet der Farbentuichtigkeitin zusam- environmentalchamber for your mengesetzen Auge von Notonecta glauca. particularneeds in the controlof Zeit. Vergl. Physiol. 29: 638-676. II light,temperature and humidity. Schildknecht,H. 1970.The defensive chemis- We offera complete line of try of land and water beetles. Angew. table-top, reach-in and walk-in Chem. (Int. Ed.) 9: 1-19. chambers for incubationand Scudder, G. G. E. 1976. Field studies of the plant, animal and tissue studies. flight muscle polymorphismin Cenocorixa Due to theirunique design (Hemiptera,Corixidae). Verh. Int. Verem. and construction,they can be quickly Limnol. 19: 3064-3072. installedand easily adjusted to your individualneeds. Scudder, G. G. E., and J. Meredith. 1972. And to accommodate the changing requirementsof scientificinquiry, Temperatureinduced development in the Sherer can also provide you with tailormade environmental"rooms" indirectflight muscles of adult Cenocorixa. in 96 standardmodels and virtuallyhundreds of modifications. Dev. Biol. 29: 330-336. So call or write today for your copy of our new catalog.And find Thorpe, W. H. 1950. Plastron respirationin insects. Biol. Rev. 25: 334-390. out how to gain controlof your environmentalcontrol problems. aquatic Rheem ManufacturingCompany, RefrigerationProducts Division, Wr6blewski,A. 1958. The Polish species of Kirk. 1100 Memorial West Columbia,South Carolina29169, Telephone the genus Micronecta (Heteroptera, Drive, Ann. Zool. 17: 247- TWX810-666-2103. Corixidae). (Warsaw) 803-796-1700, 381. SHERER Young, E. C. 1965. Flight muscle polymor- phism in British Corixidae:ecological ob- CIRCLE NO. 57 ON THE READER'S SERVICE CARD servations.J. Anim. Ecol. 34. 353-390.

500 BioScience Vol. 31 No. 7