Download Environmental adaptation to lagoon systems

OC EANOLOG ICA ACTA, 1982, N' SP
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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-
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