Survey
* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
SMS 322 Biology of Marine Vertebrates Spring 2001 Vertical distribution, vertical movement, buoyancy control February 15 Reading assignment: Helfman et al. pages 45, 63-65, 185, 296-298, 308; Reynolds and Rommel pages 25-26, 33, 34-35, 36; Berta and Sumich page 190. 1. I titled this lecture vertical distribution, vertical movement, and buoyancy control, but I intend to talk mostly about buoyancy control and how it may or may not constrain vertical distribution and movement. a. b. c. d. e. 1. Preface: many marine vertebrates move 10s to 1000s of meters vertically on a regular basis, while others restrict activities to a very narrow vertical range. Some of those tied to the surface to breathe, nevertheless, make dives down to 100s to 1000s of meters to feed, e.g. seals and penguins. Some of those not tied to the surface make daily movements upward to feed by night and downward to avoid predation by day, e.g. many mesopelagic fishes. In contrast, many deep sea bentho-pelagic fishes may remain with a meter or two of bottom for much of their lives. Apologetically, at the beginning, lecture will focus on fishes because they are so well studied with respect to buoyancy. Mentioned previously that water is much more dense than air, so gravity is not such a big issue as it is for terrestrial or aerial vertebrates–but it is there. a. b. c. d. Density of sea water is about 1.026 kg l-1 and that of fresh water about 1.000 kg l-1, plus or minus depending on temperature and salinity. Densities of most tissues of marine vertebrates are greater than that of sea water, and so, obviously greater than that of fresh water. Table in handout gives some densities of tissues from three unrelated bottom dwelling fishes, two teleosts and one elasmobranch. Note that the skeletal elements of the shark are less dense than those of the teleosts but still greater than the density of sea water. (See Table I of Pelster 1997.) Thus, in the absence of other adaptations, marine vertebrates would tend to sink. i. ii. For benthic dwellers not tied to the surface, this tendency might well be an advantage to exploit. For water column dwellers or for those tied to the surface to breathe, the tendency to sink must be overcome by some mechanism requiring the input of metabolic energy. 1 a. b. 1. Pelagic marine vertebrates have evolved three basic mechanisms for partially or completely overcoming the tendency to sink: hydrodynamic lift (as discussed last time), gas-filled “balloons” within the body, and incorporation of non-gaseous low density material within the body. A term: if an organism’s density just matches that of the environment, we say the organisms is neutrally buoyant and there is no tendency to rise or sink in the water column. Not all marine vertebrates are neutrally buoyant by any means. Let’s start with fishes with regard to these three mechanisms. Here again, the fishes are more well studied than the other marine vertebrates. a. Hydrodynamic lift, I mention just briefly. i. ii. iii. a. Pelagic vertebrates that are neutrally buoyant do save the added energy that tunas and sharks have to expend, so there is some energetic advantage to neutral buoyancy. i. ii. iii. iv. a. Many of the continuous fast swimmers use their pectoral fins, and to some degree their keeled caudal peduncles and asymmetrical caudal fins as hydrofoils to provide lift. Examples are tunas and some sharks. If the animal swims continuously for other reasons (e.g., seeking food), the added energy requirement to provide the lift is not great. However, there is a chicken and egg question: do tunas swim continuously because they will sink otherwise, or do they rely on hydrodynamic lift because they swim continuously for other reasons? My guess is primarily the latter. If the higher density of most vertebrate tissues is compensated by introduction of a low-density structure, the needed volume of the organ depends on its density. The larger the difference between body density and buoyancy-structure density, the smaller the volume needed to compensate. Because pressure and viscous drag both increase with body volume, it is energetically advantageous for the volume of the buoyancy device to be small. So logically, one is led to gas-filled structures as the lowest density inclusions conceivable, short of a vacuum. Gas bladders or swim bladders of teleosts fit the bill as low density gas-filled inclusions. 2 i. ii. In sea water, teleosts need a gas bladder of about 5% of total body volume to achieve neutral buoyancy. In fresh water, the value is about 8%. So this covers the range from estuarine to oceanic fishes. There are disadvantages to using gas bladders to achieve neutral buoyancy, and one is of energetics and one is of stability. The energetic disadvantage is greater, the deeper the fish. The stability disadvantage is greater, the shallower the fish. (1) (2) (3) Gas bladders are flexible structures, and Boyle’s law tells us that the pressure and volume of the bladder will vary directly with hydrostatic pressure. Hydrostatic pressure increases about 1 atmosphere per 10 m of depth. At the surface the pressure is 1 atm and at 1000 m is 101 atm. Consider a fish in neutral buoyancy at 10 m deep. (a) (b) (c) (1) The unstable condition is greatest near the surface. (a) (b) (c) (d) (1) If it moves up slightly, the gas bladder expands slightly in response to Boyle’s law. This makes the fish less dense than the water (i.e., positively buoyant), and it tends to rise further. If the fish moves down slightly from 10 m, the bladder contracts slightly, making the fish more dense than the water, and it tends to sink further. The situation is a positive feedback loop, which is inherently unstable. If a fish at 10 m moves to the surface, the hydrostatic pressure is reduced from 2 atm to 1 atm, and the gas bladder will double in volume. If the fish moves from 10 m to 20 m, the gas bladder volume will decrease by 1/3 (2 atm to 3 atm pressure). In contrast, if a fish moves from 1000 m to 990 m or to 1010 m, the gas bladder volume change is small, so the tendency to keep rising or sinking is also small. Regardless, the fish is in neutral buoyancy at only one depth. To retain neutral buoyancy during vertical movements, the fish must restore gas bladder volume, by resorbing gas while or after ascending and by secreting gas while or after descending. The energetics disadvantage is greatest in the deep ocean. 3 (a) (b) While it takes less of a volume change to compensate for a 10 m descent in the deep sea than near the surface, the amount of gas needed to accomplish it is much greater because of the enormous pressure. However, the volume of a gas bladder needed to accomplish neutral buoyancy (in absence of other compensations) is much greater in the deep sea. (i) (ii) (iii) i. Fishes with gas filled bladders have been found between 5000 and 7000 m deep. The density of oxygen (main gas in bladder) at these depths is 0.6-0.65 kilograms l-1. Density of air at surface ~1.2 grams l-1. Many teleost fishes with well developed gas bladders do maintain neutral buoyancy. How do they regulate gas bladder volume? Briefly. (See Fig. 4 in Pelster 1998.) (1) (2) The gas bladder is an elongated outgrowth of the esophagus that lies in the dorsal part of the body cavity. The connection to the gut (pneumatic duct) is maintained in many shallow dwelling, primitive teleosts (salmon, eels), a so called physostomous condition. (a) (b) (c) (1) (2) (3) In physostomes, it is possible to come to the surface and swallow air to inflate the gas bladder or to compensate for loss by diffusion across the bladder wall. It is also possible for these to release gas through the pneumatic duct when rising in the water column. From earlier comments, you’ll realize that this strategy doesn’t work except very near the surface. A fish would have to have a very large balloon at the surface (making it positively buoyant) to allow neutral buoyancy even at a few meters deep (Boyle’s Law again). In the more advanced teleosts, the pneumatic duct is lost during development, the so called physoclistous condition. In these, and in many physostomes, there is a mechanism for secreting and absorbing gas that does not depend on surfacing. Secreting of gas into the gas bladder occurs in a specialized structure called a gas gland. (a) The essence is a rete mirable, i.e., a network of 4 (b) (c) capillaries supplied with oxygenated, arterial blood. The capillaries are arranged as a counter-current exchanger. The gas gland cells secrete CO2 and lactic acid, which causes two effects. (See Fig. 9 in Pelster 1998.) (i) (ii) (iii) (a) (b) (1) As blood flows away from the bladder in the exchanger, gases diffuse from the outgoing capillaries to the incoming capillaries in a multiplier effect. As the partial pressure increases to greater than that in the gas bladder, the gases will diffuse into the gas bladder, inflating it. Because the partial pressure of gas in the gas bladder is greater than that of the surrounding water, there is loss of gas by diffusion across the bladder wall, which must be minimized to be effective. (a) (b) (1) Acidification causes hemoglobin to unload its oxygen rapidly. Acidification also causes the solubility of oxygen and other gases in plasma to descrease. These effects cause the partial pressure of the gases to rise in the plasma. The swim bladder wall contains guanine and hypoxanthine crystals, which reduce diffusional loss by about 100 times. In some species, this is an ontogenetic mecahnism. For example, adult American eels, which are about to leave shallow fresh waters for a somewhat deeper oceanic migration, increase the guanine content of their swim bladder wall by about 1.5 X. An ascending physoclist (and some physostomes) needs to resorb gas to remain neutrally buoyant. (a) (b) (c) In these, there is a separate area of the gas bladder wall or along the pneumatic duct where there is a bed of capillaries not arranged in a counter current system. This area is supplied with venous blood. Some means of isolating the area from, and exposing the area to, the bladder is needed, usually a muscular 5 sphincter of some kind. i. Our knowledge of increasing pressure with depth, would lead us to speculate that the rete mirabile should be more well developed in deeper dwelling fishes. Is it? Yes! (1) (2) (3) (4) (5) Rete lengths of epipelagic fishes typically 1 mm long Upper mesopelagic fishes 1-2 mm. Lower mesopelagic fishes 3-7 mm. Baythpelagic fishes that have gas bladders 15-20 mm long. Further, there can be appropriate ontogenetic modifications. (a) (b) (c) a. The American eel, when undergoing changes in preparation for its oceanic spawning migration, increases its retial length from about 2 mm to about 5 mm (2.5 X). Retial cross sectional area increases by 1.5 X. Counter current exchange efficiency increases 3.4 X. Fishes, now including cartilaginous fishes, have evolved non-gas based mechanisms to reduce their body density to achieve or approach neutral buoyancy. i. ii. One big advantage of non-gas based mechanisms may now be apparent. They are non-compressible, so a neutrally buoyant fish is neutrally buoyant at any depth (almost), i.e., buoyancy is stable. These mechanisms fall into three categories: accumulation of low density lipids, development of watery tissues, and reduction in skeletal density and total skeletal mass. (1) Reduction in skeletal density and skeletal mass. (a) (b) (c) (d) Density. The elasmobranchs all have cartilaginous skeletons. Density of cartilage about 1.05-1.13 kg l-1, while that of teleost bone is about 1.3-1.6 kg l-1. The skeleton of the lumpsucker, a neritic teleost, is cartilaginous and almost uncalcified. Its vertebral column density is about 1.05 kg l-1. Even those with bony skeletons may decrease the amount of mineralization, i.e., the content of heavy ions such as Ca, phosphate, sulfate. Three neutrally buoyant notothenioid Antarctic fishes have ash contents of <0.6% of skeletal mass, compared to 0.7-3.8% in other members of the same family. These species also have considerable cartilage in the skull, pectoral girdle, and caudal 6 (e) (f) (1) skeleton. Mass. In some deeper dwelling Antarctic fishes (e.g., Pleurogramma antarctica), the vertebrae are just very thin rings of bone around a persistent notochord; neural and haemal spines are reduced, ribs are very small. Deep sea fishes typically have reduced skeletons, and many are without scales. Accumulation of lipid. (a) (b) (c) (d) (e) Many lipids have densities less than that of sea water, so accumulation of substantial amounts reduces total body density. (See Table II in Pelster 1997.) Many unrelated groups accumulate lipids for buoyancy reduction and regulation. Lipid accumulation occurs in gas bladder, liver, bone, muscle, beneath the skin, and extracellularly. Extreme lipid accumulation gives rise to the common names of some species, e.g., the castor oil fish and the candle-fish, which have lipid contents about 20% of wet weight. Many deep sea fishes and many mesopelagic fishes have partially or completely lipid filled gas bladders. (i) (ii) (1) Some deep sea fishes have functional gas bladders filled with oxygen, but also have large amounts of cholesterol in the bladder wall. Cholesterol is denser than sea water, and is present to reduce diffusional loss of oxygen. Other bathy- and meso-pelagic species have low density lipids (typically wax esters) in the gas bladder, e.g., among unrelated species, the coelocanth, myctophids, the orange roughy (Family Trachichthyidae). Development of watery tissues, briefly. (a) (b) (c) Tissue fluids of teleost fishes (but not elasmobranchs) are hypo-osmotic to sea water, i.e., they are less dense. Thus, accumulation of large amounts of tissue fluids could reduce density. The lumpsucker, already mentioned, has muscle density of 1.024 kg l-1 compared to the typical teleost value of 1.06-1.08 kg l-1. Subcutaneous gelatinous deposits occur in 7 lumpsuckers, some deep sea sharks, and non-migratory mesopelagic species. i. As an informative example of comparative buoyancy, we could consider the endemic Antarctic family Nototheniidae. (1) (2) (3) (4) i. As another informative example, we could consider some sharks, whose livers are large and contain lots of lipid. (1) (2) (3) (4) (5) 1. 2. Some species are benthic, some bentho-pelagic, and some pelagic. All lack a gas bladder. The percent dry weight that is lipid and the percent wet weight that is water is given in the accompanying table. The table indicates the habitat and apparent neutral buoyancy. (See data from Eastman 1998 and Friedrich and Hagen 1994.) All lack gas bladders. Typical teleosts have livers that are 2-4% of body weight, while those of sharks may be 20-25% of body weight. One study of 11 species of sharks caught in the Caribbean between 275 and 530 m deep is summarized in the accompanying table. (See data from van Fleet et al. 1984.) The table indicates relative size of liver, percentage body weight as lipid, and apparent neutral buoyancy. To confirm that liver lipid plays an important role in buoyancy regulation, a couple of authors have performed simple but elegant experiments. They put small weights on sharks, and within a few days the sharks had increased the ratio of lower density lipids to higher density lipids. The reptiles, birds, and mammals are much less studied than the diversity of fishes. I’ll make a few comments. These other groups will get their revenge when I talk about diving in a few periods. Turtles and sea snakes. a. b. c. Turtles, like birds and mammals, have gas filled lungs, so they have a built in balloon, but this balloon is compressed upon diving as is fishes. Hatchling and early juvenile loggerhead and green turtles (at least) are positively buoyant and dive only to a few 10s of cm or a meter or two with difficulty. As they grow, turtles apparently become close to neutral buoyancy at least at shallow depths. They regulate lung volume to achieve this. Addition of weights or floats to yearling loggerheads were quickly compensated by lung volume changes. 8 d. e. Adults not studied, but they do sometimes bask at the surface, suggesting positive buoyancy, probably adjustable by lung volume. Sea snakes (here Pelamis platurus) often lie motionless at the surface near floating material waiting for prey. This suggests positive buoyancy, but they do dive as well. i. ii. iii. iv. v. 1. Some of the aquatic birds have been studied, especially in relation to diving behavior and energetics. a. b. c. Sea birds that rest at the surface of the ocean (most) are all clearly positively buoyant at that time. They have lungs, and they depend on air trapped in the feathers for insulation. Some of the ducks, loons, grebes, murres (and of course penguins) dive to considerable depths for feeding (more anon). Studies by Lovvorn et al. on diving ducks show that buoyancy forces are much more important than body drag in the locomotor cost of shallow diving or swimming underwater. i. ii. iii. iv. v. vi. vii. 1. I found one laboratory study in which the density/buoyancy of sea snakes was measured experimentally under several conditions. Sea snakes have a single long lung extending from trachea to anus. Those resting at the surface were highly positively buoyant, 0.48-0.56 kg l-1. Those beginning a dive were still positively buoyant, 0.76-0.85 kg l-1. Those resting at the bottom of the tank were slightly negatively buoyant, 1.075 kg l-1. Remember density of sea water at about 1.026 kg l-1. For canvasbacks, redheads, and lesser scaup, body volume increased linearly with body mass. (See Fig. 2 in Lovvorn and James 1991) Work against drag was 10-12% of total locomotor cost. Work against buoyancy was 36-38%. Work to accelerate body during unsteady stroking was 49-54%. Lungs and plumage air do get compressed as bird dives, but apparently many remain positively buoyant at all depths to which they commonly dive. (See Fig. 8 in Lovvorn and Jones 1991.) The table included here gives values for a variety of species to emphasize that they are all buoyant to some degree. (See data from Lovvorn and Jones 1991 and Lovvorn et al. 1999.) Across many species, body volume increased linearly with body mass. (See Fig. 2 in Lovvorn and Jones 1991.) Mammals. 9 a. b. c. d. Marine mammals have apparently not had any systematic study. Some at least have positive buoyancy, prompting Kooyman (1973) to note “A seal floating upright in the water rides about as high as a man in a life vest.” They do have lungs, and most have blubber, lipids with densities less than sea water. The degree to which these contribute to buoyancy has not been calculated. It has been argued that marine mammals might need increased density to overcome the buoyant forces from lungs and blubber. i. ii. iii. a. b. Increased bone density might so function. Sirenians do have bones of very high density. Cetaceans and some pinnipeds have reduced bone density. Some marine mammals have lungs greater than predicted based on body size (e.g., sea otters, which spend a lot of time floating on their backs). Others that are deep divers have smaller lung (e.g., Weddell seals, bottlenose whales). (See Fig. 2-12 in Pabst et al. 1999.) Sea otters have similarities to the diving birds in that their fur traps a layer of air. Between the air in lungs and trapped in pelage, they have substantial work against buoyancy. 10