© 2001 by The Society for Integrative and Comparative Biology
Role of Behavior in Meeting Osmotic Challenges1
1 Department of Marine, Earth and Atmospheric Sciences, Box 8208, North Carolina State University, Raleigh, North Carolina 27695-8208
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 SYNOPSIS INTRODUCTIONOPTION 1. "CHOICE": SELECTION...OPTION 2. CHANGING FACTORS...OPTION 3. EXPLOIT (POST-RENAL)...OPTION 4. SELECT AN...OPTION 5. CREATE AN...CONCLUSIONS TO BE DRAWN...References |
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Biologists must remember that physiology is the product of natural selection on organisms interacting with heterogeneous environments. "Behaving" organisms may alter the osmotic conditions they experience and achieve results unexpected from laboratory studies. Their ability to exploit environmental heterogeneity depends on its temporal/spatial scale relative to that of the organism, and the correspondence between the osmotic differences and the organism's sensory and osmoregulatory physiology. "Behaviors" include evasion of stressful habitats, selection among differing microenvironments, changing body characteristics that affect salt/water uptake/loss, manipulating fluids differing in osmolytes, and modification of osmotic microenvironments (especially for vulnerable offspring). To draw "comparative and integrative" inferences, investigators must strive to understand an organism's actual challenges by "seeing" the world from its perspective, and then making observations and performing experiments in the context of the "real world" experienced by that organism.
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INTRODUCTION |
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SYNOPSISINTRODUCTIONOPTION 1. "CHOICE": SELECTION...OPTION 2. CHANGING FACTORS...OPTION 3. EXPLOIT (POST-RENAL)...OPTION 4. SELECT AN...OPTION 5. CREATE AN...CONCLUSIONS TO BE DRAWN...References |
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Osmoregulation, the maintenance of a more-or-less constant intracellular osmotic milieu for proper functioning of cellular biochemistry, confers advantages over osmoconformity (intracellular concentration dictated by that of the external environment). Enzyme systems can be optimized for constant, predictable conditions rather than having to operate (sub-optimally) over as broad a range of concentrations as occurs in the environment.
Osmoregulation can be accomplished by manipulation of ion and water exchange across the general body surface, as may occur in organisms without obvious osmoregulatory organelles or organs (e.g., Hydra). It is becoming increasingly clear that even in unicellular organisms, the osmotic work usually is performed by specialized areas of membrane. Whether the osmoregulatory responsibility is general or localized, however, the osmotic work required, and the risk of osmotic damage, can be reduced if the organism can alter the immediate osmotic environment with which it must deal. In other words, behavior can be an important contributor to osmoregulation, if the environment presents osmotic heterogeneity.
"Behavior" is (to paraphrase Webster) "acting, functioning, or reacting in a particular way ..." In reviewing behavior's roles in osmoregulation we therefore focus on "skin-out" phenomena, providing selected examples of how organisms "act, function or react" to exploit osmotic heterogeneity in their environments. Two caveats: first, "behavior" is not always easily distinguishable from "physiology," especially in unicellular organisms, plants and sessile animals that appear to have few "choices"; and second, "behavior" is not always obvious to us when it is being performed by organisms very unlike us in habits, body form or environment.
What represents "environmental heterogeneity" to an organism? It depends on the spatial scale of the heterogeneity relative to the organism's size and its range: how large a piece of the world is accessible to its senses? to its membranes? It also depends on the range of osmotic variation relative to the organism's sensory physiology (it cannot exploit what it cannot detect), and to its osmoregulatory physiology (all portions of the environment that exceed the organism's lethal limits will kill it equally dead.)
To understand osmoregulation of organisms in the real world, then, we must remember that organisms are more than bags of interesting molecules or vehicles for sets of genes. They interact with their environments, and the genetics of behavior and physiology are the result of selection in that context. We must consider, too, that "behavior" may provide options that will not show up under laboratory conditions, and thereby affect either water or osmolyte budgets, on either the intake or output side.
To formulate reasonable hypotheses about how behavior could contribute to osmoregulation, we must learn to see the organism's microenvironment(s) from its point of view (to loosely paraphrase a doctrine imparted to generations of students by Rudy Ruibal, our mentor at the University of California-Riverside). We must bear in mind its sensory, physiological, and locomotory abilities. Or, as the late Ralph I. Smith drummed into us at U.C. Berkeley, "Ask the question in a way that the organism can understand!"
What kinds of behavioral options (either default patterns or adaptive overrides) do organisms have to alter their water and osmolyte budgets, and thereby meet osmotic challenges? We have collected some examples intended to alert our colleagues to the kinds of "tricks" that organisms can use, interacting with their environments to enhance their osmoregulatory capabilities beyond what might be seen under laboratory conditions.
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OPTION 1. "CHOICE": SELECTION AMONG MICROENVIRONMENTS DIFFERING (TEMPORALLY OR SPATIALLY) IN OSMOTIC CHARACTERISTICS (I.E., AS SOURCES/SINKS OF IONS OR WATER) |
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SYNOPSISINTRODUCTIONOPTION 1. "CHOICE": SELECTION...OPTION 2. CHANGING FACTORS...OPTION 3. EXPLOIT (POST-RENAL)...OPTION 4. SELECT AN...OPTION 5. CREATE AN...CONCLUSIONS TO BE DRAWN...References |
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It must be emphasized that such choices only represent "behavior for meeting osmotic challenges" if the environmental scale, and the organism's size and mobility, permit it to partition time among several potentially stressful microenvironments with differing costs and benefits, and to assemble over time a more optimal composite osmotic environment. Maintaining homeostasis by simply abandoning stressful habitats, while a "behavior," is not the same as "meeting" the osmotic challenges while remaining within a suite of such habitats.
Temporal (e.g., seasonal, daily) heterogeneity in availability of water vapor or liquid water provides osmotic "choices" even for sessile plants and animals.
Plants exploit diurnal differences in atmospheric water potential to maximize inward diffusion of CO2, without increasing transpiration of water, a smaller molecule. A dramatic example is the halophytic iceplant Mesembryanthemum crystallinum, which is capable of switching from C3 metabolism to CAM (crassulacean acid metabolism), a pathway allowing incorporating of CO2 into malate in the dark. This allows the plant to open its stomata at night and take up CO2 while atmospheric water potential is higher. During the day, when evaporative demand is high, it closes stomata, and metabolizes the accumulated malate (reviewed in Winter and Smith, 1996
).
Various terrestrial invertebrates (e.g., molluscs, isopods, land crabs [Wolcott, 1988] and amphibians [Jorgensen, 1997]) also exploit diurnal differences in water potential, being crepuscular or nocturnal, and restricting activity (e.g., foraging) to times when humidity is highest.
Among the most spectacular exploiters of diel and longer-term variability are tenebrionid beetles of the Namib Desert (Hamilton and Seely, 1976; Seely and Hamilton, 1976; Seely et al., 1983). These mostly nocturnal or crepuscular animals are excellent water conservers, spending much of their time buried in desert sand, where interstitial humidities are high. The exception is the large Onymacris unguicularis; these beetles are mostly diurnal and usually bury at night. Both they and the more nocturnal species emerge from the sand in response to (or even in anticipation of) the coastal fogs that occasionally form at night and dissipate the next morning. Standing tail-up at the top of dunes, O. unguicularis "fog bask" while wind-borne water droplets coalesce on their bodies and run down to their mouths. During a single fog they can replace 12% (max 34%) of their body weight, whereas on fogless nights, they typically lose 1.14% (Hamilton and Seely, 1976). Other species build "fog traps," pushing up sand ridges perpendicular to airflow, then move back along them, flattening them to extract the collected condensate (Seely and Hamilton, 1976).
Other desert animals also exploit diel variation. Small desert mammals typically are nocturnal, minimizing water loss by retreating to humid burrows by day, at the expense of greater thermoregulatory cost during cold nights. Desert reptiles, by contrast, are typically active by day, when atmospheric water potential is lowest. The higher diurnal temperatures permit them to maximize performance of their muscular and digestive systems, but at the expense of greater water loss. If they are unable to obtain sufficient water from food, they too remain inactive in humid burrows by day (Dunlap, 1995).
Desert amphibians (anurans), belonging to a group that typically has evaporative loss rates similar to those of a free water surface, have drawn much attention. The spadefoot toad Scaphiopus couchi is tightly tied to seasonal variation, burrowing during the dry months and compressing its entire annual activity (foraging and breeding) into July–Sept, the months of summer rains (rev. Jorgensen, 1997). An analogous lifestyle has been adopted by the amphibious crab of Australian deserts, Holthuisana transversa. It emerges from its burrows only during transient floods, which may be separated by one or more years (Greenaway and McMillen, 1978).
Temperature, like humidity, also varies over the day–night cycle in deserts. Large desert mammals (dromedary camels) store heat throughout the day, allowing body temperature to rise rather than spending water to tightly regulate it, then dump heat by convection, radiation and conduction at night. Small diurnally-active desert animals (lizards, ground squirrels) do much the same thing on much shorter time scales, behaviorally thermoregulating by shuttling between sun and shade or burrow; among the benefits is prevention of excessive evaporative loss from overheating (Schmidt-Nielsen, 1975).
Sporadic availability of free water is an important form of temporal heterogeneity. Not surprisingly, organisms that inhabit dehydrating environments often are able to respond with behaviors that allow rapid re-hydration when water is temporarily available. Dehydrated desert anurans have a "water absorption response" that allows them to absorb water at 30% of body weight per hour (rev. Hillyard, 1999). Similarly, dehydrated desert tortoises regain lost weight, lower their blood concentration to normal levels, and replace bladder stores of dilute water during brief rainstorms. Such re-hydration events occupy a tiny fraction of the animal's life and are easy to miss; a single good drink every year or two may suffice (Peterson, 1996). Even large desert mammals have similar behaviors; dromedary camels can rapidly drink and absorb huge volumes of water (to 30% of body weight at one draught) (Schmidt-Nielsen, 1975).
Another behavioral aspect of re-hydration is the storage of dilute urine as a water depot, and an ion or osmolyte dump. This behavior is typical of terrestrial anurans (e.g., Australian Cyclorana platycephalus can store in their bladders a volume of water equal to half their total weight (Jorgensen, 1997). Desert gopher tortoises also store dilute urine that buffers evaporative loss and allows them to hold blood osmotic concentration constant, at least until bladder contents become isosmotic with blood (Peterson, 1996). The store of dilute urine in their bladders contributed to the decimation of Galapagos tortoises; thirsty sailors, even if not in need of meat, would kill tortoises just for their "canteens" (Jorgensen, 1998).
Temporally modulated behaviors involving selection and handling of food also can contribute to osmoregulation. Kalahari desert springbok (Antidorcas marsupialis) do not drink. They typically forage shortly before dawn, when forage plants have the highest moisture content, reducing their osmotic challenge well below what would be expected by researchers who collect their samples of forage plants by day (Nagy, 1994).
Spatial heterogeneity in availability of water or ions provides options for mobile animals, and occurs at many scales. For aquatic animals, selecting a microenvironment of tolerable concentration is possible where osmotic gradients exist at useful scales, as in estuaries or the coastal ocean. Planktonic larvae spawned in estuaries may distribute themselves vertically around salinity gradients in such a way that truly estuarine species are retained, while those that complete development in oceanic water are carried offshore. However, negative feedback mechanisms that could "regulate" position are rarely clear (Cronin, 1982; Mann et al., 1991; Chen et al., 1997). Nekton (strong swimmers) clearly exercise choice over long time scales (for instance, anadromous or catadromous fishes that divide their life history between fresh and salt water). Osmoregulatory adjustments do not appear to be the driving factors, though; instead, they are adaptations that permit a migratory response to other selective forces (e.g., predation pressure or food availability). Unlike air-breathers, water-breathing animals are in constant intimate contact with their medium. This may account for the paucity of examples in which water-breathers exploit one microhabitat to store up water or ions for use in another of differing salinity, even if they have the mobility to move quickly between them.
Animals that live at the edge of the sea are presented with particularly pronounced spatial osmotic heterogeneity. The mangrove tree crabs Aratus pisonii inhabit the canopy, where they lose several per cent of their body weight to evaporation over a few hours. They periodically climb down mangrove roots to the water surface to re-hydrate. The re-hydration behavior may be overlooked because it often is so fast; the water surface is dangerous and the crabs immerse their bodies for only 1–2 sec (Wilson, 1985). A. pisonii is preyed upon by the crab Goniopsis cruentata in the intertidal, and by fish when it is in the water; it dives from the canopy only as a desperate maneuver to escape from avian predators (Warner, 1967; Diaz and Conde, 1989).
Where osmotic characteristics of food are spatially variable, food-selection and -handling behaviors again can contribute to osmoregulation by maximizing input of required water or osmolytes. Marine bony fish and toothed whales live in a hyperosmotic medium, and much of the potential prey is hyperosmotic (osmoconforming invertebrates). Many of these species derive a "water bonus" by eating bony fish whose osmotic concentration resembles their own (selective "behavior" or evolutionary specialization?). Selection of food items is much clearer among desert antelope ground squirrels Ammospermophilus leucurus and jackrabbits Lepus californicus, which excel at finding bits of succulent forage widely-dispersed among dry plants (Nagy, 1994).
The most spectacular example of food selection are the desert kangaroo rats Dipodomys merriami. These small rodents have exceptionally low water loss rates due to a respiratory countercurrent heat exchanger, highly-concentrating kidneys, and a low basal metabolic rate. They harvest seeds from the desert floor, transporting them back to the burrow in external fur-lined cheek pouches that preclude absorption of salivary water into inedible seed coats. In chipmunks, with internal cheek pouches, losses can amount to 60% of the preformed and metabolic water available from the seeds harvested (Vander Wall, 1993). Kangaroo rats select seeds yielding the maximum amount of preformed and metabolic water (Frank, 1988; Nagy and Gruchacz, 1994), even if not dehydrated and even if starved (when energy-maximization might be expected). Apparently, water above the minimum requirement saves energy that would otherwise have to be spent on concentrating urine. Finally, kangaroo rats cache the seeds in humid burrows, where they absorb enough additional water to meet about 20% of the rodents' water budget. The net result of these behaviors is that kangaroo rats maintain water balance in harsh desert environments without drinking at any season (Nagy and Gruchacz, 1994).
Selection of food may serve to optimize uptake of osmolytes as well as of water. Moose and other ungulates often forage on aquatic vegetation; in some cases this clearly is not just a means of acquiring a more easily digestible energy source, but a response to "sodium hunger." It supplements the scarce Na+ in their "normal" (terrestrial) foraging environments (MacCracken et al., 1993; Moe, 1994). The use of salt licks by a variety of species is a familiar phenomenon. Even insects may visit locally concentrated sources of ions like brackish seeps or the urine and dung of larger animals.
Drinking water, like food, can vary spatially in osmotic characteristics and present options for selection behaviors that contribute to osmoregulation. This phenomenon has been particularly thoroughly studied in land crabs, which often occur in habitats containing both seawater and freshwater. Robber crabs Birgus latro drink by spooning up water with their chelae (Combs et al., 1992; Taylor et al., 1993). When hydrated, they select freshwater and seawater in about equal volumes. However, when dehydrated (hemolymph concentration >1,050 mOsm/kg) they show a distinct preference for freshwater, thereby lowering hemolymph concentration, and raising wet weight, back to normal.
Christmas Island red crabs Gecarcoidea lalandii, when hemoconcentrated by evaporative losses, similarly prefer freshwater in which to partially immerse themselves, thereby bringing down hemolymph concentration (Combs et al., 1992). Hemodilution also can occur because urine flow and ion fluxes are fairly high despite mechanisms to conserve ions. Since the only free water is rain and dew, the major source of replacement ions is the diet. During the crabs' migration to the shore to breed, they presumably do little foraging, and become hemodiluted. As soon as they reach the shore they spend several hours "dipping" in the sea and making up the ion and osmotic deficit before moving to the breeding grounds. After breeding, they "dip" again before undertaking the migration back inland (Greenaway, 1994).
In contrast, the little red Caribbean land crabs Gecarcinus lateralis rarely enter seawater. They are such accomplished ion-conservers (see urine reprocessing, below) that they are able to maintain osmotic balance by drinking rain and dew and feeding on inland vegetation (Wolcott and Wolcott, 1988). Ghost crabs Ocypode quadrata forage on the open beach and were thought to make up evaporative losses by occasionally entering the sea. However, we observed individuals living away from the shore for a week or more, stimulating the search for alternative water sources and the discovery of the behavior by which ghost crabs extract interstitial water from sand (Wolcott, 1976). Throughout their range, from within a few meters of the surf to several hundred meters inland, the interstitial water is virtually fresh. This provides an adaptive explanation for the animals' hemolymph being substantially hypo-osmotic to seawater. Indeed, once we understood their behavior, we realized that their osmoregulatory challenge most of the time is conserving ions, not obtaining water (Wolcott, 1984).
Choice of drinking water from osmotically different sources is highly developed in some vertebrates. Laboratory rats, when rendered hypovolemic by subcutaneous injection of colloid, selectively drink saline and de-ionized water in proportions that make up a solution isosmotic to blood. The choice is being exercised even before there has been time to absorb what has been drunk, suggesting central nervous processing of sensed salinities (Stricker et al., 1992).
Migration is another behavior that can make available remote sources of drinking water or of osmolytes that are not available in the local environment. From personal observation and the popular literature, almost everyone is aware that ungulates and elephants trek to water holes and salt licks, sometimes over substantial distances that imply excellent spatial memory. Desert birds live in environments far from water sources, depending on their ability to fly fast and relatively cheaply to maintain water balance. Similarly, coastal ducks exploit both the energy-rich but salty forage of estuaries, and the fresh water of inland ponds, by shuttling between them (Adair et al., 1996). Even more ungainly animals like the marine toad Bufo marinus (rev. Jorgensen, 1997) and the Galapagos tortoise (rev. Jorgensen, 1998) migrate hundreds of meters to ponds or springs to re-hydrate and replenish their stores of dilute bladder urine.
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OPTION 2. CHANGING FACTORS (BODY CHARACTERISTICS) THAT DETERMINE RATE OF WATER/SALT GAIN/LOSS |
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For plants, modifying form is one of the few "behavioral" options. The best examples are among the halophytes, which may alter their leaves and roots under hypersaline conditions (review by Lovelock and Ball, 2001). They commonly decrease leaf size, which decreases solar heating by increasing surface:volume ratio, and speeds the uptake of CO2 by decreasing thickness of the boundary layer through which it must diffuse. In the extreme cases, leaves are dropped during stress, and over evolutionary time they may be reduced to scales (e.g., Salicornia spp.) or dispensed with completely. Leaves also are modified in response to saline stress by increasing their angle to solar radiation, which further reduces heating. Their cuticle may be increased in thickness to reduce non-stomatal water loss. This, and adoption of C4 metabolism, help to maximize the ratio of C assimilated to water used. Water consumed in transpiration must be replaced from soil, and if the soil water is saline, plants must deal with excess osmolytes as well as limited water. Many halophytes exclude salts from the root system. Their ability to minimize transpiration becomes even more important if the soil conducts water poorly, because extraction of water, but not salts, from the root zone would lead to local increase in concentration and further increase the plant's load. The plants still must deal with that fraction of the salts that cannot be kept out of the transpiration path. Some halophytes excrete salt from leaves; others sequester salt in the leaves (raising their osmotic potential and ability to maintain turgor when water must be drawn up from saline soil), then get rid of it by "discard excretion" when leaves senesce and drop.
Animals, being mobile, have additional options. When confronted by desiccation stress, terrestrial species exhibit a variety of behaviors that reduce airflow across evaporating surfaces, or reduce heat input. These include slowing or stopping the ventilation of respiratory surfaces; and clumping, huddling or burrowing to both minimize the body surface exposed to drying conditions and to maximize humidity in the microenvironment.
Intertidal marine animals face a particularly stringent osmotic challenge when the tide drops and they are exposed to an essentially terrestrial environment. Bivalves and barnacles avoid contact with that environment, not by running away but by sequestering themselves from it by tightly closing their impermeable shells. This minimizes water loss, but raises an alternative set of challenges: these animals, isolated from the atmosphere, have various mechanisms for dealing with hypoxia or anoxia. Some limpets "home," returning at every low tide to a specific site that the margin of their shell has grown to fit exactly. It was thought that this behavior was an adaptation for desiccation resistance analogous to the closed shells of bivalves. However, a closely related non-homing species achieves just as low a desiccation rate by secreting a mucous membrane between shell and rock. The "lock-and-key" fit of homing limpets may have more to do with resistance to dislodgment (Wolcott, 1973) than with desiccation. Intertidal species with permeable integuments are obliged to find tolerable microenvironments at low tide. Isopods and amphipods (Moore and Francis, 1985) spend low tide buried in wrack, where variation in temperature and humidity is strongly damped relative to the exposed intertidal surface. Finding such refuges is especially important for the smallest individuals.
Terrestrial amphibians face a challenge analogous to that of marine intertidal animals, in that they are highly permeable animals in a potentially desiccating environment. Under conditions unsuitable for activity, they typically decrease evaporative area by huddling against the substratum with the limbs held tightly against the body (rev. Jorgensen, 1997). Alternatively, they seek a shelter or burrow that provides shade and/or high humidity (e.g., the Indian tree frog Polypedates maculatus hides in banana shoots during day; Lillywhite et al., 1998).
The osmotic state of an animal is affected by the use of evaporative cooling. A variety of species use it facultatively, only when the water loss is affordable. The Indian tree frog Polypedates maculatus, which begins to "sweat" at 30°C, basks to body temperatures as high as 38°C when hydrated, but avoids direct sun and microenvironments above 30°C when dehydrated (Lillywhite et al., 1998). As noted earlier, Dromedary camels relax thermoregulation and allow their body temperature to rise during the day when conserving water (Schmidt-Nielsen, 1975).
In estuarine and intertidal environments, organisms may be subjected to abrupt changes in the osmotic environment, as when the ebbing tide brings nearly fresh water over an essentially marine community. A common behavioral response, especially among bivalves and barnacles, is to "clam up," closing the shell and minimizing osmotic impact of the stressful medium by limiting its contact with permeable tissues (Davenport, 1985). Obviously, this behavior is effective only if the imposition of stressful conditions is temporary, since the animal cannot conduct gas exchange or feeding while tightly closed.
Organisms lacking impermeable "shells" may have the option of altering the permeability of their integument to minimize osmotic exchange in water, or to reduce or replace evaporative water loss in air. Sea anemones expel water and contract tentacles when subjected temporarily to stressful salinities, minimizing their surface area. They may also secrete copious mucus as a practical osmotic barrier. On land, the "waterproof frogs" discovered by Ruibal and colleagues (rev. Jorgensen, 1997; Lillywhite et al., 1998; Hillyard, 1999) achieve evaporation rates as low as those of desert reptiles by secreting lipid-bearing mucus and elaborately smearing it over their skin. While aestivating in burrows, lungfishes reduce evaporation rates by secreting a cocoon of mucus; amphibians reduce theirs by an order of magnitude by incorporating successive layers of shed stratum corneum into their underground cocoon (rev. Jorgensen, 1997).
Changes in permeability can also affect the intake side of budgets. Terrestrial anurans, prompted by the same renin/angiotensin system that controls oral drinking in other vertebrates (Hillyard, 1999), "drink" transcutaneously by increasing the permeability of a posterior area of ventral skin and pressing this "pelvic patch" to moist substrata or free water (rev. Jorgensen, 1997).
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OPTION 3. EXPLOIT (POST-RENAL) URINE AS AN OSMOTIC POOL HAVING CHARACTERISTICS DIFFERENT FROM THOSE OF THE GENERAL MEDIUM |
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There are indications that some species reprocess urine to reclaim water. Small edaphic arthropods, although living in soil interstices that typically have humidities within 2% of saturation (rev. Villani et al., 1999
), still sustain evaporative losses that must be made up. Recirculation of urine seems to be used by terrestrial isopods (from maxillary glands, via capillary channels, to the pleopods where water is reabsorbed) and collembola (from labial nephridia, via a ventral groove, to the ventral tube where water is reabsorbed). Terrestrial mites have similar conduction systems, but their role is not well understood.
The reprocessing of urine to reclaim ions has been well-demonstrated in land crabs. Although ghost crabs Ocypode quadrata and Caribbean red land crabs Gecarcinus lateralis cannot osmoregulate when immersed in fresh water, in air they can maintain blood osmotic concentrations for weeks with access only to de-ionized water (as damp sand for O. quadrata, drinking water for G. lateralis). This led us to the hypothesis that terrestrial crabs have the option of directing isosmotic urine to organs that, unlike the antennal gland, are capable of producing strong gradients. Indeed, when hemodiluted crabs of either species are held without disturbance, they discard a "final excretory product" ("P") that is markedly hypo-osmotic to hemolymph. This urine-reprocessing behavior has been demonstrated both in crabs that inhabit dry burrows (Ocypode, Gecarcinus; Wolcott and Wolcott, 1985, 1991) and in Cardisoma guanhumi, which routinely immerse themselves in a pool at the bottom of their burrows and might be expected to osmoregulate like other aquatic crabs (Wolcott and Wolcott, 1984 and in preparation). The urine is passed backward into the branchial chambers, and over 90% of the salt (as Cl–) reabsorbed before the "P" is discarded. It now appears that reprocessing of urine into "P" is a universal characteristic of land crabs worldwide.
Robber crabs B. latro produce "P" by reclaiming ions via the gills, as well as ingesting part of the urine and/or "P" (Greenaway et al., 1990). When the osmotic concentration of the drinking water is raised from de-ionized water to 300 or 600 mOsm/kg, rates of drinking and "P" production, and concentration of "P," rise dramatically—sometimes within a day. The mechanisms for ion conservation or excretion are so effective and flexible that B. latro probably never needs to exercise its ability to selectively drink saline water (Taylor et al., 1993).
The large volumes of dilute urine retained by some terrestrial (especially desert) species may also be used as a solute dump as well as a water depot. Desert gopher tortoises continue to excrete nitrogenous wastes into the bladder during the extended periods during which water is unavailable, dumping the accumulation when occasional rains (separated by a year or more) make water available (Peterson, 1996).
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OPTION 4. SELECT AN OSMOTIC MICROENVIRONMENT SUITABLE FOR DEVELOPMENT OF (PRESUMABLY LESS-CAPABLE) YOUNG |
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Adults of nektonic (strongly-swimming) species commonly migrate to appropriate osmotic environments for young before reproducing. Anadromous (e.g., salmonids) and catadromous fishes (e.g., eels) are well-known examples. Mobile invertebrates also perform similar migrations; female blue crabs Callinectes sapidus may move 200 km from foraging and mating areas in upper Chesapeake Bay to high-salinity spawning grounds near its mouth (Millikin and Williams, 1984
). The young of many species, especially aquatic ones that use estuaries as nursery areas, also make ontogenetic shifts in habitat. These may be related to developing osmoregulatory abilities, but predation pressure or food availability clearly play important roles (Morgan and Christy, 1995).
Providing an adequate osmotic milieu for young includes avoidance of microenvironments damaging to eggs or larvae. When their eggs are mature, female land crabs Gecarcinus lateralis migrate to the sea to release larvae. Eggs will hatch in any salinity, even fresh water, and migrating females assiduously avoid all standing water (rain puddles, tidepools), thereby avoiding the loss of prematurely hatched larvae to media in which they could not survive (Wolcott and Wolcott, 1982).
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OPTION 5. CREATE AN OSMOTIC MICROENVIRONMENT APPROPRIATE FOR SELF, EGGS AND YOUNG |
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Adult land hermit crabs, by selectively taking up the appropriate proportions of fresh and salt water into the snail shells they inhabit, surround themselves with an osmotically optimal portable microcosm (Greenaway, 1988
). Such an osmotic microcosm can be created for young only when they are brooded in a chamber that allows isolation from the general medium. In some amphipods, the fluid in the brood chamber is actively regulated at an osmotic concentration intermediate between those of the medium and of the brooding female's hemolymph (Morritt and Spicer, 1996; Morritt and Richardson, 1998), apparently by channeling isosmotic urine into the marsupium. Similar phenomena occur in terrestrial and euryhaline aquatic isopods. The cladocerans are excellent osmoregulators, occurring in freshwater to hypersaline environments. Some species have closed brood pouches, the contents of which the parthogenetic female strongly regulates at about the same concentration as her own hemolymph. When the larvae become able to osmoregulate, the female relaxes regulation and allows the fluid to become essentially isosmotic with the medium (Aladin and Potts, 1995). The brood pouches of male sea horses and pipefishes (syngnathids) are maintained at the concentration of the fish's blood, and have been hypothesized to serve a similar osmoregulatory function for larvae. Larvae of Syngnathus scovelli explanted into sterile, non-nutritive artificial seawater survive nearly as well at 875 mOsm/kg (hyper-osmotic to blood and pouch fluid) as at 363 mOsm/kg (isosmotic), suggesting that the pouch has no essential osmoregulatory role. However, small sample sizes suggest that larvae grow larger in the pouch and under isosmotic in vitro conditions, hence that parental osmotic regulation may provide an energetic saving and thereby foster faster growth (Azzarello, 1991).
In some terrestrial crabs, the regulated microcosm is not even part of the adult's body. The Jamaican bromeliad crabs Metopaulias depressus rear their young for 2 mo in the water pools of bromeliad axils. Axil water tends to have intolerably low pH, insufficient calcium to support larval development, and oxygen tensions that fall below lethal levels at night. Females remove organic debris, thereby keeping oxygen above the minimum for larvae to regulate metabolism. They also collect snail shells that they add to the axil in which their larvae are living, increasing pH to tolerable levels and providing sufficient Ca++ for incorporation by larvae (Diesel and Schuh, 1993). This represents regulation, not mere addition; females respond to experimentally-induced low Ca++ by increasing their collection of snail shells 5-fold, thereby raising pH and doubling the Ca++ concentration (Diesel, 1997). Other small Jamaican mountain crabs, Sesarma jarvisi, use a less-obvious nursery: empty snail shells lying in rock crevices (Diesel and Horst, 1995). Their porous limestone (karst) habitat rapidly drains away surface water. Small potholes may hold water long enough for crabs to molt, but not to undergo larval development. Females produce 3–24 extremely large (1.3 mm) eggs, and release them into snail shells that they have filled with water they have transported (presumably in their branchial chambers) from elsewhere. They tend the larvae for 2–3 mo in these nurseries. The water starts out clear, but gradually becomes muddy and acquires various plant and animal parts, suggesting that females actively provision their broods (although direct observations are lacking). Undoubtedly the addition of tissues to the water has effects on the osmotic microenvironment of larvae, but until measurements are made it is only possible to speculate on whether females "regulate" it.
Nestling birds also inhabit a microcosm isolated from surrounding osmotic environments; they have no access to free water other than rain. Consequently, the composition of food provided by attending adults is a major determinant of their osmotic state. Adult white ibis Eudocimus albus normally forage primarily in salt marshes, obtaining mostly fiddler crabs; however, while provisioning nestlings they spend up to 13 times as much energy flying to freshwater foraging habitats, where they obtain mostly crayfish and bony fish having half the osmotic concentration of fiddler crabs. Excessively salty food depresses growth rates and survival, and rarely is fed to young. After the young fledge, the adults shift foraging back to saltmarshes (de Santo et al., 1997).
Conversely, precocial chicks feed themselves, but their osmotic milieu is affected by where parents take them. Adult piping plovers Charadrius melodus perceive (without much apparent justification) that ghost crabs Ocypode quadrata are a threat. Where crab populations are high, the adults restrict foraging of the brood to backshore and dune areas that provide little moist food. The low fledging success on such beaches apparently is not due to predation, and may result from dehydration (Wolcott and Wolcott, 1999).
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CONCLUSIONS TO BE DRAWN FROM THIS ECLECTIC LIST OF EXAMPLES |
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SYNOPSISINTRODUCTIONOPTION 1. "CHOICE": SELECTION...OPTION 2. CHANGING FACTORS...OPTION 3. EXPLOIT (POST-RENAL)...OPTION 4. SELECT AN...OPTION 5. CREATE AN...CONCLUSIONS TO BE DRAWN...References |
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First, what human scientists see is not necessarily the environment experienced by other organisms. Our sensors are designed for sub-aerial use, and are of little use in non-terrestrial environments. Most of them are nearly 2 m from the ground, and suited to observing macroclimate, not the microenvironments of species much smaller than we are. We tend to be diurnal, especially in work habits, whereas many organisms do their most interesting things at other times. Finally, what humans find pleasant or aversive may be quite irrelevant to other organisms. The net result: we may not instinctively grasp what phenomena represent the real environmental challenges to another species.
Second, if we are unaware of the options presented to organisms by their normal environment, we may explore phenomena like osmoregulation under conditions that do not allow "normal" behaviors. An organism without the normal options may not be able to do its normal "end runs" around chemistry or physics. The result may be a gross misjudgement of the organism's capabilities—a classic example is the conclusion that [immersed] land crabs can survive only a few hours in fresh water, when in nature they routinely live for months with access to no other water source.
In summary, then, biologists who wish to interpret the natural world must make special efforts to understand it from the organism's perspective. We need to grasp what the organism's real challenges are, and what its real options are, so that we can "ask it the question in a way that it understands." To do this well, we must look beyond our preconceptions and our own narrow specialties. We truly need to be "Integrative and Comparative Biologists."
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FOOTNOTES |
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1 From the Symposium Osmoregulation: An Integrated Approach presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 4–8 January 2000, at Atlanta, Georgia.
2 E-mail: tom_wolcott{at}ncsu.edu
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