* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
Download Environmental adaptation to lagoon systems
Survey
Document related concepts
Latitudinal gradients in species diversity wikipedia , lookup
Human impact on the nitrogen cycle wikipedia , lookup
Habitat conservation wikipedia , lookup
Biogeography wikipedia , lookup
Biological Dynamics of Forest Fragments Project wikipedia , lookup
Soil salinity control wikipedia , lookup
Theoretical ecology wikipedia , lookup
Renewable resource wikipedia , lookup
Microbial metabolism wikipedia , lookup
History of wildlife tracking technology wikipedia , lookup
River ecosystem wikipedia , lookup
Transcript
OC EANOLOG ICA ACTA, 1982, N' SP ~ ----=~-'-'------'----~- Environmental adaptation to lagoon systems Lethal limils Multiple factor interaction Encrgy budgets Physiological adaptation Limites létales Interaction multifactoricllc Budgets énergétiques Adaptation physiologique F. J . Vcrnbcrg Belle W. Baruch InslÎtute for Marine Biology and Coaslal Rcscarch, University of South Carolina , Columbia, South Carolina 29208, USA. ABSTRACf Environmental adaptation to lagoon systems Organisms rcsiding in lagoon systems on a permanent or transient basis have cyolvcd numcrous adaptivc ploys to mect the evolutionary challenge of a dynamic cnvironmc nt, including functional , behavioral and morphological rncchanisms. The lagoon cnvironment not only consists of .. normal ,. biolie and abiotic factors , but the number and types of « maninduced,. factors arc increasing rapidly. Hence polluants and pelturbations arc now a permanent palt of Ihis habitat type. The dynamics o f organismic-environmental interaction involves lethal and sublet hal responses of ail life cycle stages. Various physiologieal systems not only arc independent ly adapted 10 envi ronmental changes but intcrsystcm inlegration has oceurred. The principal purposes o f this paper arc 10 review brieOy exist ing literature , to highlight sorne current research trends, and to attempt a synthesis of integrative mechanisms. The principal e mphasis is on individual species, as community metabolism , will be diseussed elsewhere , but symbiotic relationship and population characteristies will be diseusscd. Oceallol. Acta, 1982. International Symposium on eoastal lagoons, SCORlIABO/UNESCO . Bordeaux, France, 8-14 September •. 198 1, 407-415. RÉSUMÉ Adaptation environneme ntale aux systèmes lagunaires Les organismes lagunaires , qu'ils soie nt des résidents permanents ou temporaires , ont développé de nombreuses stratégies d'adaptation en réponse aux mult iples sollicitations de l'environnement. Ces adaptations portent su r des mécanismes fonctionnels , comportementaux ct morphologiques. l 'environnement lagunaire présente en plus des paramètres abiotiques ct biot iques «normaux ,., un nombre croissant de paramètres imputables à l' homme. Il en résulte que dans de nombreu x cas, des pollutions et des perturbations d'origine anthropiques fonl désormais partie intégrante de l'habitat lagu naire. La dynamique des rapports qui règlent l'adaptation des organismes à leur milieu est telle qu'e lle implique des réponses adaptatives pour lutter contre des conditions létales ou scmilétales à chaque étape du développement. l'évolution a favorisé le db'e loppement de mécanismes adaptatifs d'ordre physiologique répondant spécifiquement aux sollicitations du milieu mais aussi celui de mécanismes complexes intégrés. Cette revue a pour bul principal de résumer l'état présent des études, de meure en relief quelques tendances actue lles de la recherche ct de synthétiser nos connaissances relatives aux mécanismes imégrateurs au niveau de l'espèce. Les rappons symbiotiques ct les caractéristiques adaptatives de populat ions SOnt éga lement passés en revue. Acta, 1982. Actes Symposium International sur les SCORlIABO/UNESCO, Bordeaux , 8·14 septembre 198 1, 407-415. Oceanol. lagunes côtières, has been describcd as bcing hostile , demanding, or physi· cally stressed when compared to more stable environments, such as thc dcep sea. Hence , o rganisms in lagoons would bc expected 10 dcmonstrate a widc array of adaptations to the numcrous physical , chemical , and biological factors which comprise this ecologically interesti ng segment of the Earth's INTRODuc nON AnimaIs and plants residing in the coastal lagoon habitat , eithcr as permanent residenls or as lransicnts duri ng various seasons of the year, face a complex o f cnvironmental factors cach of which may vary widely. Traditionally this habitat Contribution Numbc r 435 from the Belle W. Baruch Institule , Unive rsily of Sout h Carolina. 407 F. J. VERNBERG biosphere. Although biologists frequent ly stud y the influence of one or a few environmental factors at a time, wc must nOI forget that many factors may vary independently or in concert to affect an organism. Recognition of the dynamic inlcraclion betwcen an organism and its c ntire environmental complex is refcrred to as the principle of the holocoemic envi ronmc nt (see review. Billings, 1952). As background for devcloping the theme of this ge neral review paper , functional adaptation to the lagoon habitat , the dynamic interaction between the internai functioning of an organism and its external milieu must be recognized. For discussion the environment commonly is subdivided into two major componenls: 1) abiotic faclors, and 2) biotic factors. The abiotic compo nent consists of various physical, geological , and chemical factors . such as oxygen, temperaturc , sediment, geomagnetism , pressure , and pH, while the biolic eomponent includes ail interorganismic relationships, such as competition , predator-prey relationships, and symbiosis. Sorne factors arc not easily classified as e ither biotie or abiotic; for example, a metabol ite (chemieal fac tor) produced by one organism may act as a prey attraetant when released to the external environ ment (biolic interaction). Internally, the va rious physiological proccsscs of an organism arc influenced to varying degrees by cha nges in extemal facto rs. This paper will present a few selected examples of how o rganisms living in lagoons respond to thdr external environmenl. For each speeies a cenain sector of the potential range of expression of an environme ntal factor is compatible with life. At cit her end of Ihis range or gradient there is a point beyond which an organism is unablc to survive. The broad middle sector of a gradient has been given various narnes : the zone of compatibility, the zone of tolerance, the biokinetie zone, or the zone of capacity adaptation. The region at either end of the zone of compatibility i5 called the lethal zone or the zone of resistanee. The point of transition between these two zones is referred to as the upper or lower incipie nt lelhal point. The upper and lower incipient lethal points arc defined as that exposure level which ki lls a Slated fraction o f the population ( usually 50 %) within an indefinite ly prolonged exposure. This point of transition bet.....een the zones of resistance and eompatibility is difficult to characterize , since facto rs sueh as sex, season, slarvation, or interaction of various environmental factors may ca use il to vary. At the onset of this paper, it is necessary 10 delimit thc use of the term environmental adaptation bccause it is a term whieh has been used in 50 many wa ys Ihat it has limited deseriptive value. Evolutionary adaptation connotes a genetic basis for adjustment among the paTIS of an organism and belween the organism and its environ ment (Allee el al. , 1949). Within the existing ge nome of an organism , adaptive morphologieal, bchavioral, and/or physiological responses to environmental stress may aceur and need not rcly on mutations. Sorne biologists rcfcr to these reslX' nses as nongcnetic or environmentally induccd adaptation. Physiologieal adaptation. as viewed by Prosse r (1975), is « any propcrty of an organism which fayors survival in a specifie environrncnl, panicularly a stressful one ". He includes in this definition both environmentally and gcnelically delermincd responses. Two terms used in discussing differences in responses of organisms are environmentally induced ( phcnotypic) variation and genolypic variation. The respon· ses of an individual organism to a ce rtain environ mental complex may be labile. ln ordcr to de termine whether an observed response of an animal is nongenetic or genetic, certain expcrimental approaches have been used: 1) the breeding and rearing of organisms under differenl environmcntal conditions Ihat arc controlled ; and 2) acclimation studies in which reslX'nses of organisms exposed to a new environmental condition arc observed. In the present dis· cussion, physiological adaptat ion will be equaled with environme ntal adaptation. This paper has the followin g major objectivcs : 1) to present an overview of earlier studies and 10 review recent resea rch on environmental adaptation to coastal lagoons ; and 2) tO suggest some f"ture research needs. Because of limitations on the length of the present paper and the voluminous literaturc on this subject, many exciling papers cannot bc citcd. 1 hope my colleagues who are not included will bc understanding and forgiving. OVERVIEW OF PAST STUDIES Early naturalists recognized the uniqueness of organisms being restrieled to specifie modes of existence. Semper (1881) and Davenpo n (1897 and 1899) re viewed the pre20th ccntury literature on {unetional, behavioral , and morphological adaptations to various habitats, while Allee et al. (1949) su mmarized thc literature for the first half of this ccntury. These works arc not restricted to coastal lagoons , but deal with many habilats. A classie contribution to coastal lagoon sciences is the book of Remane and Schliepcr ( 1971 , Second edition) ",niology of brackish water " with the firSI edit ion appearing in 1958. In 1964 an international con ference on estuaries was hcld and the proccedings edited by Lauff were published in 1967. A comprehensive review of estuarine rescarch was prescnted , including the subject of adaptation. Other recenl symlX'sia proceedings and books have relevance to the theme of this paper : Vernberg and Vcrnberg, 1972; Vernbcrg, 1975 ; Wiley , 1976 ; Kinne , 1977 ; McLusky and Berry , 1978; Stancyk , 1979 ; Vernberg and Vcrnberg, 1981. In general, the principal lincs of rcscarch described in these references have emphasizcd the lethal limits of organisms and sublethal (zone of compalibilit y) responscs, including respiration , ionic and osmoregulation , and other funct ional responscs. CU RRENT RESEARCH Since World War Il an ever-increasing research effon in ail aspc:çu of çoastal lagoon science has takcn place. EX<:Implt.:s of a few dominant research directions in the field of environmental adaptations follow . ullwl zone The lethal effects of temperature , salinity, oxygen , Hz$, and desiccation arc abiotic factors which have received considerable attention. Temperature AnimaIs living in cold-water lagoons generally survive lower le mpe ratures than animais inhabiting warm-water habitats while the reciprocal responsc is noted al etevalcd thermal levcls. AI50 animais, ..... hich arc typicatly exposed to marked seasonal thermal changes, are better able to su rvive a wider range of temperaturcs than those organisms residing in a region of relative thermal stability. Funhermore, the upper and lower thermal lethal points of organisms from widcly nuctuat ing thermal regimes ca n be shi ft cd more widely with thermal acclimatization than organisms from more temperature-stable environments (Vernberg, 1981 ). Within one lagoon, organisms may evade high or low thermal stress by behavioral ploys. For example , if the tempe rature is too high , intenidal snails cluster and the body temperature of o rganisms in the center may be 5 to 6 oC cooler than arnbienl levels (Rohde, Sandland , 1975). Boddeke (1975) repon ed that shrimps (CrangQn crallgoll) leave eoastal cmbayments in the Netherlands during the autumn for the o ffshore watcrs of the North Sea. This migration allo .....s animais 10 inhabit the warmer ..... inter waters offshore and avoid frozen inshore lagoons. This responsc is correlatcd with the relative inability o f this species to osmoregulate at the low winter temperatures within the lagoons (Spaargaren, 1971). In addition , Boddeke (1975) found other factors to be imponant : fluctuatio ns of water temperatures in the 408 ENVJAON MENTAl ADAPTATION TO LAGOON SYSTEMS autumn initiatcd the off-shore migration, especially of sexuaUy mature animais_ Thermal resistance of adults may bc similar to that of developmental stages (Andronikov, 1975) or they may differ. For examplc, larvae of certain tropical fidd lcr crabs survive lowcr tcmperaturcs than adults, whereas , adult fidd lcr crabs from the temperate zone have widcr thermal limits than the ir larvae (Vern berg, Vernberg, 1975). Gable and Croker (1978) rcportcd that ovcr-wintering, immature amphipods showed the bcst tolerance to low temperature and salinities, while juvenile forms live closer to their upper Icthal thermal limits. Earlier PateJ and Crisp (1960) dcmonstrated a relationship betwee n upper lethal the rmal limits and the temperature range during the breeding season ; spccies from colder waters bred at lower temperaturcs and had lower upper Ihermal limits than did species inhabiting warmer-water e nvironments. ln the case of the common mud-flat snaîl (Nassorius obsolerus), the adult , inhabiting mud-flats which may be anoxie pcriodically , is more resistant to oxygen de pletion than is the more aquatic larvae (Vembcrg, Vembcrg, 1975). Desicca/ion ln genc ral organisms inhabiting the higher regions of the intertidal zone survive increasing desiccation better than those o rganisms living lower in the intertidal zone or subtidal1y (sec review, Vernbcrg, 1981). A few examples are cited here. Young (1978) reported that the most terrestrial of three speeies of estuarine hermit crabs lost body water more slowly when subjected to low moisture conditions than two subtidal specics; similar findings for subtidal and intertidal decapod crustaceans have been reported (Ahsanullah, Newell , 1977). Recently Priee (1980) examined the water relations of a salt marsh snail (Melampus bidenUlIUS) which represents a transitional stage in the movement of molluscs from the marine environment to land and fre shwater habitats. When exposed to dry conditions in the field , this species had 15 % less body water compared with specimens from moist sites. In the laboralory, it could withstand 0 % relative humidity extremely weil. For exampic , aft er exposure for 27-36 hours, the LDSG value was near 80 % body water loss. Rehydration occurs rapidly : within 0.75 hours oc normal ,. body water content of 90 % was reaehed from a level of 50 % water loss. Bascd on latitudinal distribution , Hilbish ( 1981) reported that populations of Mefampus from the more northerly locations of Massachusetts and Delaware were more resistant to freezing than were animais from South Carolina. This geographieal difference did not disappear aft er laboratory accJimation expe riments nor did transfer of animais from South Carolina to field conditions in the twO northern sites alter Ihis pattern of response. T his suggested the existence of al least two physiological races. A gencrality to he drawn from this and related st udies is Ihat funclional responses of a species living within onc lagoon may bc diffcrcnt from those of a populatio n of the same species living in another lagoon having a different range of environmental conditions. Salinity Numerous reviews have summarizcd the data on salinity tolerance and the ecology of lagoon animais (Kin ne , 1971 ; Remane, Sehlieper, 1971; Vern bcrg, Silverthorn , 1979). Earlier, Remanc (1933) suggested that a eritical salinity boundary (5-8 %cl separates fresh water and marine fauna s and Khlebovich (1969) later expanded this concept by incorporating much more data. Pronounccd physiotogical changes occur within this critieal salinity boundary region, including distortion of cellular electrochemical properties, tissue albumin fraction alterations, and changcs in growth, locomotion , and osmoregulation. Typical of the evolution of rcsearch on a given environmental problem is the fi nding that a simple rclationship hetween a given factor and its influence on an organism does nOI exist ; other variables also are important. ln the past five yeaTs, numerous additio nal examples have not only documented the importance of salinity as a limiting factor, but they have stresscd the interaction of multiple factors. For cxample, although NOTS/;; and Estevez (1977) roulld a corrclation bctween the salinity tolcrance of 10 species of portu nid crabs and their distribution along a salinity gradient , ranging fro m ful1-strength oceanic sea water to the upper reaches of an estuary, other factors, such as competition, predation, and food availability were important. Earlier Croghan ( 1961) e mphasizcd the interplay bctwecn interspecific competit ion and mechanisms of osmoregulation : a species which expends less energy in osmoregulat ion may have a competitive advantage over a second species whieh is less efficient in that more energy is available for other fu nctions, such as dcfending a habitat , finding a mate, or caplUring food . Another line of research is to report on the unexpected distribution o f organ isms into eoastal lagoons. This approach is i11ustrated in a paper by Hendrix el al. ( 1981). They found that the bay squid (Loffigullcula brevis) living in Galveston Bay , Texas could survive 16. 5 %c salinity for 48 hours whercas most eephalopods arc marine stenohaline organisms. Although this species ean survive exposure to reduced salinities, it eannot osmoregulate ove r the range of 17.5 to 36 ~ salinity, a response si milar to other euryhalinc. osmoconforming eehinoderms and bivalve molluscs (Vcrn berg, Vernbcrg, 1972). Multiple factor illleraCliolt$ Although data on the influence of a single factor on an o rganism are important , most o rganisms live in an environmental complex consisting o f numerous separate factors cach o f which may vary independently of the others. Therefore to bc able to clearly delineate between the zone o f eompat ibility and the lethal zone, in order to havc mo re meaningful eeologieal interpretation of laboratory results, greater emphasis is being placed on multiple fac tor expcrimentation (sec reviews, Alde rdice, 1972 ; W. B. Vernberg, 1975 ; F. J. Vernberg, 1979). A few reee nt exa mples will illustrate Ihis important line of rescarch. Two populations o f the harpaeticoid copepod Zaus spillarus from Robin Hood's Bay, England and Oresund , Denmark were subjected to 30 combinations of temperature and salinity al differe nt scasons o f the ycaT (Hicks, 1980). Scasonal shift s in survival occurred and statistically significant geographieal differences were reported. Man-indueed environmental perturbations may influence the ability of a spccies to survive. For examp1c , low sublet hal concentrations of cadmium, a heavy metal, dramatically altercd the ability of fiddtc r erab zocae 10 withstand various combinat ions of temperature and salinity ; in the presence of cadmium, mortality was increased, salinity sensitivily was increascd, but slight ly increased tolcrancc 10 low temperalUre was noted (Vernbcrg el al. , 1974). ln 1976, Simpson published a detailed paper on factors eontro lling vert ical migration o f six species of mo ltuscs living in differe nt zonal positions along a transecl fro m the high tide mark to the sublittoral region. Generally , the habitat and zonal position arc related 10 toleranee to tempc raturc, desiccalion , and salinity, howcver, in sorne Oxygell Consistent with the correlation of the responses to te mperature and salinity and distribution in a coasta llagoon are the results on oxygen lethallimits. The correlation of rcsistanee to anoxie or hypoxic conditions and habitat is well documcnted by Theede el al. (1969) , Vernhe rg (1972), and Van Winkle and Mangum (1975). Theede el al. (1969) also showed a similar correlation with tolcrance to H;zS. Differences in anoxic resistance of different life history stages indieate variations in physiological mechanisms and also in fl uence the dist ri bution of the di fferent stages in a lagoon. 409 F. J. VERN BERG cases the laboratory-determined lethal limit was much greatcr than the degree of exposure the species would expcricnce in the field. This was clearly demonstrated in the case of limpets. But clevated tempcratures, salinity extremcs, or desiccation effects wcre dcbilitating, resulling in a higher rate of predation on the enfeebled animais. This is a good examplc of biotic and abiotic factor interaction to limit the distribution of a spccics. Simpson concluded that the invcstigator should be wary of placing too much emphasis on resulls from studies of a single factor and that synergistic effects of factors arc limiting and the effective combinations of factors may diffcr for each species or geographical population. Most of the previously citcd papcrs have deall with rclativcly short-term exposure 10 Iclhal combinations of environmental factors, times ranging from minutes to a fcw days. Howevcr, chronic exposure to a .. sublethal JO concentration of a potential pollutanl may have serious consequences to a population over a fcw generations. The term sublethal is used to describc cxposure to a given concentration of a factor which docs not rcsult in 50 % mortality or more within a defined pcriod of time. To illustrate these longterm populational effecls, the work of Vernbcrg el al. ( 1978) on fiddler crabs and mercury exposure is cited. Based on field data on population dynamics, and laboratory experimentation on lethal mercury effects on adults and larvae , and metabolic studies, Vernbcrg et al. (1978) developed a model which predicted the decrease in population sire after a four-yeaTexposure to various levels of mercury. This work not only illustrates a new trend 10 modcJ ecologieal-physiological systems, but, also, it emphasires the need to undcrstand the long-term implications of environmenlal perturbations whcn establishing pollution criteria or making decisions on environmental manipulation. 7Ane review, Jorgensen, 1976) and/or by ingesting larger particles (sec review, Pandian , 1975; and Jones , Wolff, 1981). One of the basic problems in developing an energy budget is to determine energy input to an organism. Under laboratory conditions, input has been estimated for a number of spceies but the question can be raised .. Is this what the organism cats in the field? JO. In many ca:;es the natural diet of lagoon animaIs is unknown let alone data on quantitative aspects of ingcstion. Two recent papers illustrate attempts to fill this data void. A promincnt in habitant of salt marsh systcms is the killifish, FI/ndul14s hererodirus, and its role in carbon cycling within this ecological system is thought to bc significant. To determine the source of carbon for Fundl/lus throughout the year, Kneib and Stiven (1980) measured the stable carbon isotope ratios of their muscle tissue and gut contents seasonally. This ratio, expressed as slle values, gives an indication of food source in that marsh flora which is at the base of the food chain has a widc and distinguishabic range of ratios. Thcir data indicatc that assimilated carbon probably originated from a mixture of benthic algae and Spartina ingested by prey species utilized by Fllndulus. The ratios for these prey species in July varied from - 15.6 to -17.3. The ratio for small fish diffcred from that of large fish during the warmer months, suggesting different dietary requirements. The reason for the seasonal change in muscle tissue is not known ; the authoTS suggested either a change in diet or a change associated with reproduction. Bccause many of the routine methods of determining food intake (direct observation in the field, gut analyses, or tracer studies) arc not applicable to all components of a trophie food web, Feller et al. (1979) adapted immunologie methods when studying a soft-bottom bcnthie eommunity. They were able to detecl phyletic and trophie rclationships among 20 taxa and identified trophic links which would otherwise have gone undetected. Another important component of biocnergetics is respiration. Numerous variables have been shown to influence oxygen uptake (Vernberg, Vernberg, 1972). Recently Profc~50 r Dame and 1 dcmonstralcd that Ihe ycarly n:spiration of an ad ult population of mudcrab, Panopeus herbistii, varied depcnding on whether the animais were maintained at constant, but seasonal1y represcntative tempcrature, or at cyclic temperature (Dame, Vernbcrg, in press). Wu and Lcvings (1978) also determined the rate of respiration and its contribution to the annual energy budget for barnacles (Balanus giaT/dus) during their first year after settlement. Approximatc1y 67 % of the energy was lost in respiration with egg production being the second major component at 12.3 %. The energy balance of a speeies may be different dcpcnding on where it lives. For example, Griffiths (1981) reported that the energy budget of a mussel population (Choromy/ilus meridionalis) living intertidally was distinct from that o f a subtidal population. Upper-shore mussels had a reduced growth rate and reduccd metabolism during aerial exposu re computed for the first years of growth when compared with subtidal forms. Although she calculated that the energy requirements of the intertidal population was half that of totally submerged animais, the amount of energy allotted to reproduction in both population was not rnarkedly different. Not only may energy utilization patterns vary among populations of the same species found in one geographical arca, but this response has been reported for latitudinally separated populations (sec review, Vernberg, 1962). This was shown by Vernbcrg and Moreira (1974) who reported on the differences in the metabolic rates of Eu/erpina aCUfifrons from Brazil and South earolina, USA. Anothcr functional response which has adaptive signi fi. canee in determining the success of a species in inhabiting a specific lagoonal habitat is its ability to remove oxygen frorn the external milieu. ln response to oxygcn conccntration levels, sorne specics arc oxyconformers while others arc oxyregulators with Pc values (the critical level of oxygen tension below which the or oompatibility Bctwccn the high and low lethal environmental exttemes, an organism survives, but its success will depend upon a number of factors. Of interest tO the therne of this paper is what rnechanisms have developed in lagoonal species to allow them to successfully survive. ln order to maintain life, energy is required. This is truc no matter whieh level of biologieal organization we are examining, either organisms, populations, or ecosystems. That this conccpt has received increasingly wide acceptance is seen by the heightened research activity on biocnergetics in recent ycars. Not only is the amount of cnergy takcn into an organism accounted for, but the partitioning of this energy within the individual is determined. This method of accounting for energy input and energy usage is referred to as developing an energy budget. The commonly accepted equation for estimati ng the energy budget is as follows : e = P + R + F + U, where P = Pr + P, and P, = t::. B + E. Each component may be measured in kilocalories per ann um. e is the ene rgy content of the food consumed by the population; P, the total energy produced as f1esh or gametes; PI' the energy content of the tissue duc to growth and recruitmcnt ; B, the net increase in energy content of standing stock; E, climination, or energy content lost to the population through mortalily; P" the energy content of the gametes liberatcd during spawning j R, the energy lost due to metabolism (respiration) j F, the energy lost as feces; and U, the energy lost as urine or other exudates. Obviously, the devclopment of an energy budget is a cornplex process involving determination of various functional processes. Although it is beyond the scope of the present paper to present a detailed review of biocnergetics, sorne examples of reeent studies will indicate current problems. Because energy intake is basic to organismic survival, it is not unexpected that various mechanisms have evolved in lagoonal organisms. Dissolvcd organic substances may be removed by organisms from the surrounding sea waler (sec 410 ENVIRONMENTAL ADAPTATION TO LAGOON SYSTEMS o rganism becomes an oll)'conformer) varying with differe nt factors, such as body sUe , food , molting, Iocomotor activity, and acclimatio n 10 various ox)'gen tensions influe nce metabolism (see review of Vem berg. 1972). To provide a quantitative description of the relationship between aerobic metabolism and decreasing e nviron mental oxygen levels, Mangum and Van Winkle ( 1973), using data from 31 species of aqual ic invertebrales, describcd a quad ratic binomi na l equalion which fit the data best. Bascd on this equation, they reported a ph)'logenelic trend of Încreasing regulation of aerobic metabolism in response to declining environme ntal levcls. T his tre nd could he correlated wil h the acquisition of structures by organisms Ibat would effeetive ly insulate their respi ring tissue from the surroun· ding habitat. In many of these spedes the removal of oxygen would cease long before the available supply of oxygen was exhausted , wil h those species without substantial oxygen slorage capabilities switching to anae robie pathways. Fiddler crabs, Uca pugilator and U. pugnax, living in burrows in sandy· muddy substrates, may experience low oxygen tensions when the lide is in, since the)' apparently do not pu mp waler Ihrough their burrows. These species are not only relatively resistant to anoxia, but al50 the critical oxygen tension is low: 1·3 % o f an atmosphere for inactive and 3·6 % for active crabs. The5C crabs cont inue to consume oxygen down to a level of 0.4 % of an atmosphere; in contrast, the no n·burrowing wharf crab, Suarma cinereum, stops respiring at a somewhat higher value (Teal, Carey, 1967). Alt hough direct correlation bctween ox)'gen uptake and heat production, as measured b)' calorimetric techniques, has been reponed for many animais, Pamatmat (1978) fou nd the two processes to he more or less independe nt o f each other in the fKldler cra b, Uca pugl1ax. Hence in this species and presumably in other species experiencing either hypoxic or anaerobic conditions, ecologieal energeties should be de termined by measuring heat production since " aerobie shutdown .. and a switch to anaerobic metabolism may occur whe n re latively high levels of oxygen arc prese nt. Two xant hid crabs, Pano~w hubstii and Menipp<. mercI" I1Qria, decrease their rate of ox)'gen consumption in proportio n to ambient ox)'gen levels (Leffler, 1973), however, the rate of decrease is less than that o f the blue crab (Calfinec(es sapidus). a rcspo nse appare ntl)' correlated with habitat diffe rences in that the xant hid crabs often live in mud while the blue crab docs 50 less frcq ucntl)'. Callianassa catijOrnîensis and Upogebia pugertensis, two spccies of burrowing crabs, regulate their mctabolic rates ove r a wide range of oxygen concentrations. However, Thompson and Pritchard (1969) found species differe nces that correlated with habitat differences ; Caflianassa lives under more h)'pollic conditions tha n Upogebia and has the lower metabolic rate , Ihe lower Pc value , and i5 more resistant to anoxia. Recentl)', Torres et al. ( 1977) found that C. colijOmiensis, when placed in simulated burrow condi· tions, rcgulates oxygen levels in its Immediate microha bilat by usi ng its plcopods. Body movcmenl pla)'s a large rolc in water ellcha nge bclween the surface and the burrow. Arter ox)'gcn dcprivation, the prese nce of ox)'gen may stimu late feeding and activity al the surface of the burrow. A re lated spccies. C. jamaice!lSe, which lives in estuarine mud flats in Ihe northern Gulf of Mexico whe rc hypoxK: conditions arc common, was reported b)' Felder ( 1979) to bc very lolerant of anoxia. Il exhibitcd metabolic regulation to a Iow Pc, had a low metabolK: rate , and showed toxie responses to altered ox)'gen Icnsion: all adaptations 10 an h)'poxic habitat. Whcn ellperiencing exterAal environmenlal changes, ani· mals ma)' switch from acrobic to anaerobic mctabolism (Theedc, 1973; Breteler, 1975; Spaa rga ren, 1977), as de mo nsl rated by Carcit/w moet/as. Down 10 oxygen prcssure of abo ut 20 mm Hg, this species regulates Olrygen uptake when measured al both Ire and 2O ·C (Spaargaren , lm). The gill ventilation ra te is unchanged, and the hean ra te is more or less constant until lhe oxygen tension reaches 60-80 mm Hg (Taylor, 1976) and then decreascs (Uglow, 1973). Although there is a red uction in energy production during anoxia, sufficient energy for ionic regulation results fro m a naeroblc pathways to insu re inte rnai consta nc)'. Under anoxic cond itions the Ioss of locomoto r ability makes this species vulnerable to predation, but it can withstand changing salinilies. T hese results dc monstrate that biotie interaction is potentially more limiting under anoxic conditions than arc abiotic faclors. Associated with lagoonal systems arc organisms who have invaded the adjacent high lands for varying periods of lime. T he)' show a range of responscs. Variations in the respiralory adaptations of lerrestrial crustaceans were reported by MeMahon and Bu rggren ( 1979). Birgus, Gecarcinw, and Cardisomo arc less influe n· ced b)' h)'poxia than hypcrcapnia, a response tO bc ellpected of animais living in a habitat rich in oxygen. Howevcr, the land hermit crab, Coenobita c1ypearus, was more sensitive to h)'poxia than hypercapnia. Appare nt ly this differe nce in responsc can be correlated with the continued associatio n of C. c1ypeatw with a flu id·filled mo llusca n shcll which permit· ted the erab to retain sorne aq uat ic tc ndencies. ln gene ral the respiratory pigme nts of animaIs living in regio ns of low oxygen concentrations are more ox)'ge n sensitive than Ihat of thosc living in relatively oxygen· rich habitats. Recently We lls et of. (1980) reponed the following adaptive teatures for an intertidal polyehaetc (Terebe/la haplochae(Q). Ils hemoglobin had a high affinily fo r oxyge n (PX) value of 7 mm Hg al 2<rC) and the amount of hemoglobin in the blood vessels was high. T he shape and Ihe position of the ox)'gen·bi nding curve werc sensitive to cha nges in te mpe rature, pH, and pC02 suggesting Ihat these changes facilitated oxyge n delivery du ring exposure at low tide. The ultrastruclUral architecture of the gills and blood vessels enhaneed the ra tc of oxygen diffusion fro m the external environment by permitting short diffusion distances and large surface areas. Lagoonal organisms faced with flucluating salinity regimes must ada pt or perish. Within Ihe zone of compatibility, organ isms have de monstrated various response patterns , ra nging fro m osmo rcgu lating 10 osmoconforming. Although the responsc pattern is genetically de termincd, the e nvironme nt may greatly influe nce the expression of the pattern. Temperature, sca5On, and food arc a few known variables. Gilles ( 1979) ed ited a book which compre hensivel)' dealt wit h the ionic and osmoregu latory mechanisms o f aquatic organisms in respo nse to e nvironme ntal changes. Recently, the effect of salinity on the Ionie and osmoregulalory responscs of five species o f peneid shrimp was rcported by Cast ille and Lawre nce (1981). Ali five specics responded similarily : the hemolymph is hype rosmotic to sea water at salinilies be low the isosmotic concentrations and hyposmotic to higher salinities. However, spccies diffcrences were nOled in thal Pel1Qeus azteclIs and P. duorarum were weaker ionic and osmoregulators at low salinities than the othc r thrce spccies. This respo nse ma)' bc corre lalcd wit h the distribution of these shrim ps: P. aztecllS and P. duorarum arc least abu nda nt in lower sa linities. Alt hough shri mp regu larl)' inhabit coasta l lagoons, most cephalopods live in C08stal waters over thc continental shelf. One exceplion is the bay squ id Lolliguncu/a brevis which may invade coastal bays and lagoons, however, it is not weil adapted to an estua rinc existence in that it is an osmoconforrne r over the range of 17.5 to 36 %c> and shows signs o f severe osmotic stress in sa linities be low 17~ (Hcndrix et al. , 1981). The response of Carcinus when subjccted to sudden changes in salinil)' was dctcrmined by Ta)'lor (1977) ; Ihe carlier work was do nc o n animaIs acclimated to low salinilies. In nature, this crab is frequcntly subjected to ma rked flu ctuation in salinity si nce it livcs in estuaries and in rock pools. Afte r exposurc to reduced sali nit y the oxygen consum ption mtes we re highest du ri ng the ensuring 2·3 hours, after which they declincd. Howeve r, the rate was a lways highe r than thal reponed du ri ng the periods befoTe exposure to low 411 F. J. VERNBERG salinity. This increased oxygen consumption rate lasted even after 3 to 5 days in water of rcduced salinity. a resÇM::msc indicating that the respiratory rate of Carcimls docs not acclimate rapidly to rcduced salinity. ln estuaries the salinity may fluctuate rapidly with the changing tidcs. Findley el al. (1978) examined the cffects of a simulatcd tidal cycle on the respiration of two common cstuarinc spccies, the blue crab (Callinectes sapidus) and the oyster drill (Thais haemastoma). Respiration rates of ani· mals acclimated to 10,20, and 30~., salinity were measured at one temperature (20 OC) after exposure to various scmidiurnal salinity regimes (10·5- 10 %<>, 20·10-20 %C>, 30-10· 30~", and 10-30·1O'k<». Blue crab respircd more rapidly at 10 and 20%<> S than at 30%<> S. With fluctuatÎng salinity, their mctabolic rate varied inversely, although relatively minor changes occurred. Typically the respiration rate droppcd during the initial phase of declining salinity at a rate directly proportional to the rate of salinity decrease. This transitory responsc could represcnt a metabolic adjust· ment period since this spccies is capable of regulating extracellular fluid osmotic and ionic composition. ln contrast, the oyster drill exhibits ineompletc volume regula. lion and its metabolic rate was more directly influenced by salinily change. Thc mctabolic rcsponse to salinity may be an indicator of the distribution of species along a salinity gradient as illustrated in a study of two braekish water isopods by Frier ( 1976). Sphaeromil hookeri is most abundant in Danish waters in salinities below 15 'k<> and may occupy waters with a salinity as low as 2 'k<>, while S. mgicauda typically is not found in salinit ies lower than 10 'k<>. The rate of respiration is higher in S. hookeri and increascs more rapidly in low salinities than that of S. rugicauda. However, Frier rcportcd no direct correlation bctween the degree of osmoregulation and the rate of respiration as S. fl/gicauda maintained blood more concentrated at low salinities than did S. hookerj. Temperature influences the ionic and osmoregulatory abil· ity of many lagoonal spccies (sec revicw of Vernberg, Silverthorn, 1979). A (ew examples demonstralc this point. As reported in adult blue crabs by Lynch el al. (1973), juvenile blue crabs have higher haemolymph salt concentrations in cold water than in wanner water of the same salinity (Lcffler, 1975). Part of this increase is duc to inereascd haemolymph Na+ concentration. The permeability to salis of the erab, Carônus maenas, changcs with salinity. Although changes proceed more slowly at 5 oC than at 20 oC, tempcrature docs not greatly influence the final permeability (Spaargaren, 1975). The ability of an isopod (Sphaeroma serralll m) to regufate the sodium concentration in the haemolymph varicd seasonaJ1y. Ionie regulation increases with low tcmpcrature and is important during the winter (Charmantier, 1975). To be successful in the lagoonal habitat, an organism must he able to perccive changes in its external environment. At times when the waters may be murky and visual eues would bc of limited valuc, the ability to communicatc by means of sound has adapt ive value. One example of an animal using acoustical communication is the male toadfish, Opsanus lau. He produces a characterist ic boat whistle catl which acts not only as a stimulus to attract females but it probably causes ot her toadfish to leave the area where the male has established a nest (G ra y, Winn , 1961). Visual eues arc important in the life of the fiddler erabs (i.e., Uca pugilator). These crabs arc active and eompletcly cxposed in the intertidal region during periods of low tide and many of their activitics have directional components that arc adaptive. For examplc, to escape the approaeh of a predator whcn the crabs arc sorne distance from their burrow, Ihey may run landward and enter burrows or vcgctation, or they may run offshore . ln eit her cvent, the crabs arc able to orient and return to the beach, guided primarily by visual mechanisms (Herrnkind, 1968). The primary eues for guidance arc sun position and plane of polarized light, but the crabs can also use landmarks to supplement celestial cues. Fiddler crabs use both visual and acoustical signais during courtship. The displays of the males, which involve the waving of large major chetiped, arc espccially conspicuous. Recent investigations have revealed that sound production is also an important eompo· nent of courtship behavior that is distinctive for each spccies (Salmon, AtsaiJes, 1969), In U. pugi/ator, when females are absent, the crabs wave during the day and produce sound at nign!. If a (emale is nearby du ring the day, the male waves more rapidly, and if she approaches doser 10 the male's burrow , the waving is fol1owed by sound production. At nig ht a male produees sounds at low rates, but wi11 increase sound rate when touehed by a female . Females have been observed in the field ta orient and move toward males at night in response to sound from distances as great as 25 cm. Animais also rely on other scnsory modalities in their perception of the environmenl. Sorne arc able to utilize tidal sali nit y changes to their advantage in sceking a suitable cnvironment using rheotactic and chemoreceptive modaJi· ties, While reduced salinities can prevent animaIs from carrying out normal vertical migrations, changing salinities associated with the ebb and flow of the tide ean be utilizcd to advantage by olhers, such as the European ccl Anguilla vulgaris (Creutzbcrg, 1961). Salinity a!so influences the migration of sorne spccies of shrimp in and out of estuaries. ln laboratory studies on the pink shrimp Pel/Geus dllOramm, Hughes (1969) indicated that inshorc movement of post·larval shrimp and subse· quent offshore movements of juveniles were aided by flood and ebb tides, respectivcly. Man-indueed changes influence the functional responscs of animaIs living in lagoons and estuaries. For example, De Coursey and Vcrnberg (1975) reponed on the cffcets of dredging on zooplankton. T hey were exposcd to water samples taken from the Immediate area of dredging, a site 200 yards downstream, and from the disposaI region where the water drained back into the estuary through a weir. The swimming activily of zooplankton was reduced, their meta· bolism also dccreascd, and mortality rates were increascd most dramat ica11y in the« weir" water while the warer from the dredge site was least toxic. Reproductive phenomena, induding gonad development , spawning and larval dcvc1opment , arc greatly influenced by reduced and/or fluctuating salinities. Dctailed reviews of this subject arc in the continuing series « Reproduction of Marine Invertebrates" : edited by Giese and Pea rse (1974 ; 1975 : 1977 ; 1979) and a volume on reproductive ecology edited by Stancyk (1979). One example cited ta show the cffects of vanous factors on reproduction is the work of Seidel et al. (in press). The bay mysid, Mysidopsis bahia, is important in the ecoloS)' of semitropical bays and recently it has been widcJy uscd for laboratory studies of full life cyde pollution toxicity. The geographical origin of Anemia, the principal laboratory food uscd in rearing expcriments, fed to the spccies influences its survival, growth, and reproductive potentiaL For example. Anemia from five geographical locations (h aly, Brazil, Australia, and California and Utah, USA) were used. Survival was significantly lower in animais fed Arlemia from California; growth highest in mysids !cd Anemia from Utah and Brazil and lowest when fed Artemia from California. The reproductive potential was greatest in Mysidopsis fed Utah Anemia. This work illustrates the complex interaction between food , growth, reproduction and bioassay studies. FUTURE RESEARCH That lagoonal ecosystcms are important 10 human society has been well documented. However, the level of our scientifie undcrstanding of how organisms function in this ever-fluctuating environment is far from adequate to pro· vide the necessary basis for predicting the cffccts of natural and "man·related,. perturbations. Some major areas of 412 ENVIRONMENTAL ADAPTATION TO LAGOON SYSTEMS researeh which need attention are d iscussed below, but these are only a few examples. tant not only to the development of eèologieal Ihcory but also 10 dev ising modern managemcnt practices. Cooperative studies involv ing various lagoonal systems are needed in which similar data sets arc eollected and ana lyzed using comparable techniques. Synthesis studies A c rit ical evaluat ion and synthesis of published studies are needed to asscss the current state of our knowledge and to serve as a sou rce to direc t futu re research efforts. Although there is a n Inherent Ihread of continuily in ail e nvironmental st udies cncompassing a il Icvcls of biological organization, ranging from molecules to ecosystems, the coherent integration and synt hesis of the results of studies at diffe rent levcls is lacking. The biosphere fonction s as an integrated whole, and, if we want to understand how il functions , we must begin to ana lyze it as an integrated whole and not restrict our investigation to a series of isolated but detailed stu dies. Organismk studies Re latively liule is known of functiona l rcsponses of organisms subjecled 10 abiO lic and biotic conditions whieh mimie the environmental co nditions th ese organisms face in the environment. The mic rocnvironment of lagoonal organisms is poorly known : wha t are the min ute-by-minu te changes in light , oxygcn , te rnperature . and salinity that they experie nce and how would Ihese rnultifaetorial changes influence Iheir metabolism? In additio n , al1 stages in the life history of lagoonal organisms need to be studied . Larval requirements and responscs arc known 10 be different from those of the adul, for sorne species but nOI for all.why? The proble rn of what a re t he impacts of man-înduccd changes in lagoons is ever-increasing in scriousness. New compounds are constantly bcing rcleascd into t he envi ronmem : their cffects on organisms must be known. Allhough lageons have been of inle resl 10 mankind sincc pre-historie times, we have fragmentary scientific knowlcdgc of how they function. The research challenge is there and wc mUSt accept this challenge before ail we have lcft to study are estuarine dcscrts dominaled by u nending tidal forces. Intcrlagoonal com parative st ud ies As a bett er understanding emerges of various lagoonal syste ms, o ne wonders if the results are site specific or arc they applicable to ail systems. What arc the general eharaeteristies of ail lagoons and what a rc the var iability ranges o f site specifie characteristies. Are the adaptive mec hanisms enabling one lagoo n to survive perturbation the same as those of a oother lagoon? Arc the palhways of secondary production the same in t ropical, temperate, a nd polar lagoons? The answers to these ques tions are impor- REFERENCES Da"cnport C. B.. 1899. Experjmemol morphology, Vol. Il .. Macmillan , London and New York. tlre Coursey P. J., W. B. Vernberg. 1975. The effect of dredgi llg in a pollmed eSlUary 011 thc physiotogy of tarval "WOplanklUn. Watt" Res. , 9, 149·154. Felder 1). J.., 1979. Respi ra!Ory adaptations or Ihe eSlUarinc mud shrimp, Ca/liaruuso janraicelloSe (Schmitt. 1935) (CruSlacea. Dccapoda. Thalassi nidea). Biol. Bull .• 157, 125-137. Feller K. J .. Taghon G. L., Ga l la~r E. 1)., Kenny G. E., Juma rs P. A., 1979. Immunologkal methods for food web analysis in a softoonom bcnthic communit )'. Mar. Biol., .54, 61-74. Flndley A. M., Bclisle, 8 . W .. 5tlckle. W. 8 ., 1978. Effects of salinity fluctuatÎons on the respir.ltion rate of the southern oyster drill "f1rais hael1WSfOmiJ and the blue crab Caflirrecle$ sapiduJ, Mar. Biol., 49. 59·67. Frier J . 0 .. 1976. OX)'gen co nsumption and osmoregulation in the isopods Sphaeroma Irookeri Leach and S. rugicauda Leach. Ophelia. 15. 193-203. Gable 1\1 .. CrokH R. A.• 1978. The salt marsh am phipod . Gammafil S paluslris Bousfield. 1969 al thc northern limit of its distribution. II. Tempcrature-salinity tolerallccs, Estrtorille CoaSlal Mar. Sei .• 6, 225-230. Gicse t\. C ., Pearse J.5 .• cds., 1974. Reproduction of nlarille inl"/mebmll's, Vol. J, Acadc mÎC Press. New York. Glese A. C., Pcarse J. S.• eds., 1975. ReproductiQII of marine illl'er/ef)rOles. Vol. 2 IIlId 3, AcadcmÎC l'rcss. New York. Giese A. C .. Pearse J. S., cds., lm. Reprodllclio'l of murine in~erlebrOles, Vol. 4, Academie Press. New York. Giesr A. C .• Ptarse J . S .. cds .. 1979. Reproducf;mr of marùre illl'ertef)rate$, v ol. 5, Academk Press. New York. GlIlc$ R., cd .• 1979. Mulranisms of oS1lWreguioriQII in allimals. Wilcy. New York. Gray G. A., Wi nn Il. E. t 1961. Rcproduçtivc ecology and sound production of the toadfish. OpsamtS UlU, Ecolog)', 42. 274-282. Grlffit h5 R. J ., 1981. Aefial expasure and cncrgy balance in littoral and subl ittornl ChQromylilltS meridiQllolis (Kr.) (Divalvia), J. Exp. Mar. Biol. Ecol.. 52. 231-241. lIend rix J . P. Jr., lIulet W. Il .. Gru nberg M. J ., 1981. Salinity tolerance and the respo nscs to hypo-osmotÎC slress of the bay squid LolligrmC/llo brevis, a cury hali nc ccphalopod mollu.'jC. Comp. lJioclrem. Physiol.• 69A. 641·648. Ahsanullah M., Newdl R. C., 1977. Thc cffccls of humidity and tcmpcrature of watcr loss in Carcirrus matnas (L) and POr/lUrus marmoreus (Leach). Comp. Biochem. Physiol., 56. 593-601. Aldcnlice 1). F., 1972. FaÇ\or combinat ion. Rcsponscs of marine poikclotherms tO e nvi ronmc ntal faÇ\ors acting ill conccrt. in : Marine (cology, cdiled by O. Kin nc. Vol. 1. Wilcy Imerscicncc . Ncw York. 1659-1722. Allee W. C., Emerson A. E.. Park 0 .. J'ark T., Sl:hmÎdI K. P.• cds. 1949. Prillcip/es of animal u%gy. W. B. Saunders. Philadclphia. Pennsylvania. Andronlkov B. , 1975. Heat resistance of gametes of marine invertebrates in relation 10 tempcrature conditions under which the spccics cxist. Mllr. Biol., JO. 1-11. Billings W. D. , 1952. The environmental çomplex in relation 10 pianI growth and distribution. Qrllll. Rt'v. Biol .. 27. 251·265. Hoddeke R., 1975. Autumn migration and vertieal distribution of the brown shrimp CrangOIl Cfangoll L. in relation to cnvironmcnta l co nd itions. in : Nilllh European MarinI' Biology Symposium. edited by H. Barnes. Uni\'crsit)' l' ress. Aberdeen. Scotland. 483-494. Rn:telcr W. C. M. K. , 1975. Qxygen consumption alld rcspiralOry levels of juvenilc shore çrabs. CllrcinllS nwenas. in rela tion to wcight and tcmpcrllture. Nellr. J. Sea Res .. ,I. 243-254. Castille F. L. Jr., Lawrence A. Lo, 1981. The effect of salillit)' on the osmotie sodium and chloride concentrations in Ihe hemolymph of euryhaline shrimp of Ihe ge nus Perweus, Comp. 1Ji000hem. Plr)'siol.. 68'\. 17-80. Charmantlcr G .. 1975. Variations saisonnières des ca pacilés ions régulatrices de Sphaeronra serrOlr,m (Fabricius. 1787) (Crustaeea. lsopoda. I-'abc llifera). Comp. Biochem. PIr)'siol., 5OA. 339-346. Creut:dxrg F.• 1961. On the orientation of migrating clvers (AlIgrtifla ~lIlgaris lurt.) in a tidal area. Nellr. J. Sea Res.. 1. 257338. Croghan .... C.. 1961. Competition and mechanisms of osmotic adaptation, in: MtclulIIisms in biologica! competition. Symposio of the Socitt)' {or EXJXrimelllol Biology. No. 15, 156-167. llaml' R. F.. Vc rnbtrll, F. J .• 1982. Energctics of Il population of the mud crab POIIOpellS herbstii (Milne Edwa rds) in the North Inlet Esluary. Soulh Carolina . J. Exp. Mar. Biol. Ecol, 63, 183-193. Davenport C. B.• 1897. Experimerrlol morpholog)', Vol. 1.. Macmillan. London and New York. 413 F. J. VERNBERG Spaargaren D. Il., 1971. AspeÇ1s of the osmot ic regulation in the shrimps Crangon "ongon and Crangon ollnwlnlli, Neln. J. Sea res .. 5. 275·335 Spaargaren D. Il .. 1975. Cllangcs in permeability in the shore trab, Carcillus moenas, as a response 10 salînity. Comp. Biothem. Physio/.. SIA. 549-552. Spaargaren D. H., 1977. On {he metabolie adaptation of Carcinus nwmos to reduccd oxygen tensions in the environment , Nt/h. J. Seo Res., Il , 325·333. StaDl:)·k S. E" cd., 1979. ReprodUClive ec%gy ofnwr;ne im·erlebrolls. Belle w. Baruch Library in marine Science, NO. 9 Univ. South Caro1ina Press, Columbia. Ta)·lor A. C., 1976. The respiratory responses of Carcinus matnas tO decJining Oll:ygen tension, J. Exp. Biol., 65, 309-322. Taylor A. C., 1977. The respira tory responscs of Carcimu maillaS ( L.) to cha nges in environmental salinity, J. Exp. MOf. Biol. Ecol .• 29, 197-210. Teal J.M .. F. G. Carey, 1967. The metabolism of marsh crabs under tondi tions of reduced oxygen pressure, Physiol. Zoo/.. 4-0, 83·91. TlwWe Il .. 1973. Comparative swdies on the infl uence of oxygen defieiency and hyd rogen sulphi de on marine bottom in\lencbrates, Nell,. J. Seo Res., 7, 244-252. Theede Il,, Ponat A., IlIroki K.. SchlicPfn C., 1969. Studies on the resistance o f marine bottom inven eb rates to oll:ygen-deficiency and hyd roge n sulphide. Mar. Bwl. , 2. 325·337. Thompson R. K., Pritcha rd A. W., 1969. Respiratory ada ptatio ns of two burrowing Crustacea, Callralli/ssa californien.sis and Upage. bio puggetlen.sis (Dccapoda, Thalassinidae), Biol. Bull.. 136, 274287. Torres J. J. , D. L. Gluck, J . J. Cblld ress, 1977. Activity and physio logical significance of Ihe pleopods in the respiration of Callionassa œlifomie/lSis (Dana) (Crustacea: Thalassinidea), Biol. Bull., 152, 134-146. Uglow R. F., 1973. Sorne cffects of acute oll:ygen changes on hean and seaphognathite activÎty in sorne po rt unid crabs, Nerh. J. Seo. Res., 7, 447-454. van Winkle W.. Mangum C.. 1975. Oll:yconformers and Oll:yregulators. A quant itative index. J. Exp. Mar. Biol. Ecol., 17, 103· IlO. Vembcrg F, J .. 1962. Latiludinal effects on physiologieal propc n ies of animal popula tions, Alill. Rev. Physio/. , 24, 517-546. Vemtxrg F, J" 1972. Disso1ved gascs-ani mals, in: Marine ec%gy, edited by O. Kinne, Vol. l , Wiley lnterscience, New York, 14911526. Vembcrg F. J .• 1979. Multip le faClor and synergetics slresses in aquatic systems, in: Encrgy and erlVironmental stress in aquatic systems. edited by H. Thorp and J. Gibbons, Tech nical Information Center. US Dcpl. Energy, Washington , D.C., 726-748. Vcrnbcrg F. J., 1981. Benthic macrofauna, in ; FUllclio/lal adapta /iO/u of marhll OfgOIlÎSms. edited by F. J. Vernberg and W. B. Vernberg, Academie l'ress, New York, 179-230. Yernbcrg F, J .. Ver nbcrg W. B., 1975. Adaptations tO eXlTeme cnvironments, in: Physi% gica/ ec%gy of es/uarim! animais, edited by F.l. Vernberg, Univ. South carolina Press, Columbia, 165· 180. Vernbcrg F. J., Silvenhorn S. U.. 1979. Temperawre and osmore· gulation in aqua tic species, in: MeclUlllisms of osmoreglllQl;on in animais, cdited by R. Gilles, Wiley Imerscience , New York. 537562. Yembe rg F. J .. Vemberg W, B" cds., 1981. FIUIe/io'lOlodopta/ions of ma,im! orgonisms, Academie Press. New YOtk. Vernbcrg W. B.. 1975. Multiple factor effects on anima Is. in ; Pnysiological adaplolion 10 /Iu- em,ironmenl. edited by F. J. Vern· berg. CroweU-Collicr. New York, 521·538. Vembcrg W. B., Vernbcrg F, J., 1972. En~"ollml'/lIol plr)'siology of marine OIlimals, Springer-Verlag, Berlin and New York. Verube rg W, B., Moreiru G., 1974. Metabolic·temperature respon· );Cs of the copepod EmerpillO acu/ifro/IJ (Dana) from Brazil, Comp. Biochtm. Ph)'sio/.. 4\lA. 757·761. Vernbe rg W. B.• Vernberg F, J .. 1975. TIu- plrysiruogicol ec%gy of lan'a/ Nassarius obsoletus. University Press. Aberdeen, Scotland, 179-190. Yernbcrg W. B.. DcCoursey P. J .. O'lIa ra J. , 1974. Multiple environmental factor effeets on physiology and behavior of the fiddlct erab. Uca pugilalOf, in: Pof/u/Îon ond physiology ofmorim! organisms. edi ted by F. J. Vernbcrg and W. 13. Vcmberg, Academie PrcS!;. Nell' Yor k. 381-425. IIfrrnklnd W. F., 1968. Adaptive visually-di reÇ1ed orientation in Uco pugi/olor. Am. lAJo/.. 8, 585-598. IIlcks G. R. F., 1980. Seasonal and geogra phie adaptation tO tcmpcrature aOO sa1inity in the harpaeticoid copepod Zous spirnlfus spilUl/Us GoodsÎr, J. Exp. Mar. Biol. &01., 41, 253-266. Ililbish T. J., 1981. Latitudinal variation in ffeezing to1crance of Melampus bidenTaTUS (Say) (CaSfTopoda: Pulmonata), J. Exp. Mar. Biol. Ecol., 52. 283·297. lIu gbes D. A., 1969. Responses to salinity cha nge as a tidal transpon mce han ism of the pink shrimp, PelUlEus dllorornm. 8iol. 8ull. , 136,43-53. JOIlllS N. v .. Wolff W. J., cds .. 1981. Feeding a/Id sun 'ivol Slralegies of esmarine organisms. Plenum Press, New York and London. Jorgensen C. B., 1976. AuguSt Putter, August Krogh, and modern ideas on the use of dissolved orga nic matter in aquatic environments, Biol. Rel'. Cambridge Phi/os. Soc., SI, 292-328. Klmte O., ed., 1971. Salinity·i nve n ebrate animais, in; Marine ec%gy. Wiley Inte!SCience, Ncw York, 821-966. Klnne 0., cd., 1977. Ecosystc ms rc scaTCh, Hegol. Wiss. Meer(Sun· lers, 30, 1·735. Kneib R. T., Slh·en A. E., 1980. Stable carbon isotope ratios in Fundulus heleroclilUS (L ) muscle tissue and gut contents from a North Carolina Spa rtilUl ma rsh, J. Exp. Mar. Bio/. &01., 445, 89-98. Khlebovkh V. V., 1969. Aspects o f anima l evolution rclated to critical salinity and intcrnal state, Mar. 8101., 2, 338·345. ùtfIler C. W., 1973. Metabolie rate in relation to body size and envi ro nmcntal oxyge n concentration in two spedes of lI:amhid erabs, Comp. Broehem. Physlol., 44A, 1047-1052. ùtfIler C. W.. 1975. Ionie and osmotic regulatio n and metabolic responsc to salinity of juveni1e Collineeles sapidus Kathbun, Comp. Biocnem. Pnysiol., 52A. 545-549. L)"och M. I'. , Webb K, L., Yan Engel W. A., 1973. Variations in scrum constituenlS of the bluc crab , Collinee/es sapidl's: chloride and osmotic conce ntrations, Comp. Biochem. Physio/., 44, 719734. Mangum C" Van Winkle W.. 1973. Responscs of aquatic invene· braies tO dedining oxygen conditions, Am. Zoo/., !J, 529-541. McLusk)" D. S.• Berry A. J., cds., 1978. Pnysiologyand belUlvior of marine organl$ms. Pergamon Press. Oxford. Md·fallon B. R.. BUrggNn, W. w., 1979. Respiration and ~dn pla lion to the terrestriaJ habitat in the land hcrmit crab Coenobita clypea Rls, J. Exp. Blo/. , 79, 265-281. Norse E. A.• Este~·tl M. , 1977. Studies on port unid crabs from the Eastern r acific. 1. Zonation along cnvÎronmental stress gradienls from the coast of Colombi a, Mar. Biol., 40, 365-373. Pama lmat M.M .. 1978. Oxygcn uptake and heal production in a metabolic co nformer (Li/toril/o irm rata) and a metabolic regulator (Uco pugmu), Mar. Biol., 48. 317·325. Pandilln T. J., 1975. Mcchanisms of heterotrophy, in Mori!l~ ec%gy. edited by O. Kinne, Vol. 2, WiJey, New York, 61-249 l'alel B.. Crlsp D. J .. 1960. Rates of development of the emb ryos of several species of ba rnaclcs, Pnysiol. Zool., 33, 104·119. Priee C. H., 1980. Wa ter rclalions and physiological ecology of the salt marsh snail. ,\fr/ampus bidelllams Say, J. Exp. Mar. 8iol. Ecol.. 45, 51-67. ~r C. L., 1975. Physiologieal adapt at ions in animais, in: fh)'si%gko/ adaptation /0 Ilu- envirol/melll, edited by F. J. Vernberg, Intell:t EducHtional Pub[ishers. New York , 3·18. Renllne A., 1933. Veneilung und organisation der benthonischen mikrofauna der l<icler Bucht. Wiss. MeereSllfll~'S Kiel. li , 161·221. Rf mam- A., SchliePf r C., 197 1. 8i%gy of brackish waler, 2nd Edirion. \Viley. Nell' York. Rohde K.. Sandla nd R.. 1975. Factors influencing clustering in the snail Ceri/niulIl moni/iforulIl, Mar. Bio/. , 30. 203·215. Salmon M" S. l'. Atsaides. 1969. Sensitivity tO subsUHte ,·ibration in tlle fiddler crab UCII pUlfilalOT Bosc. Allim. Behol'.. 71. 68-76. SeIdel C. K., Johns D. 1'o1" Schaucr P. S.. Olney C. E" in press. IllIernational study on Anemia. XXV I The value of nauplii from reference Arremio cyStS and four geographical collections of Arte' mia as a food source for mud crab, Rhithropanopeus lUl"isil. lan.·ac, Mar. Ecol. Prog. Ser. StmPfr K, G,. 1881. Animallifo as affocled b)' Ine lIamral COlldi/ioflS of exisle/IU. Appleton , Ne"· York. Simpson R. D., 1976. l'hysical und biolic factors limiting the distribution and abundance of littoral molluscs on Macquarie Island (Sub-Antaretie). J. Exp. Mar. Biol. Ecol.. li. 11-49. 414 ENVIRONMENTAL ADAPTATION TO LAGOON SYSTEMS Vernlxl'l W. B.. MeKeila r JI. J r., Vemlxlll F. J . • 1978. Toxkity studies and enviro nmc:ntal impaC1 asscssmcnt. Environ. MallQgt· rrwn/, 2. 239·243. Weil! R. M. G .. Ja"b: P. J .. Shumway S. E.. 1980. Oxygen uptake. the drculatory system. and haemoglobin function in the inte n idal p>lychaelc Ttrtbeflo hopflxhatla (Ehlers), J. Exp. Mar. Bw/. &o/.. 46. 2SS-m. Wlky M., cd., 1976. E.J/Uarint prot:tSJtl, Vol. 1: Usel, S/rtSJts, and udap/a/ions /0 /~ ts/ua", Academie Press, Ncw York. Wu R. S. S., Ln lnp C. D. , 1978. An encrgy budget fo r individual barnacles (Hafanu.J gfadufa), Mil'. Biol., 45. 225·235. Young A., 1978. Dessiccation loleraoccs for Ihree hermit crab spedC5 ClibofllJriu.J v;(/QfU.r (Bosc). Paguru.J pollitaris Say and P. /ongitarplU Say (Dccapoda. Aoomura) in the North Inlet estuary. South Carolina, E.J/Uarint Coaslal Mllr. Sei., 6. 1l7-122. 416