Diane Campbell, Temperature and habitat effects in Dodeca ria fewkesi. p. 2 INTRODUCTION Dodecaceria fewkesi, a small cirratulid polychaete, inhabits envi- ronments ranging from the mid-intertidal to subtidal depths of at least 90 feet. Berkeley and Berkeley (1954) have reported that it forms single-sex colonies by asexual reproduction and lives in reef structures consisting of masses of calcareous tubes. Colonies from various habitats differ in the external structure of the tube masses and in the size of the animals. Any given asexual colony must have been subjected to the same environmental conditions for many decades. Because both the environmental conditions and the morphology differ between habitats, it is likely that animals from various habitats show physiological differences as well. For a wide variety of organisms, subtidal animals have higher respi- ratory rates over a wide range of temperatures than intertidal ones. Com- parisons of rates between animals from various habitats have been made for few polychaetes. Magnum (1972) has found that intertidal species of onuphids have a higher 00 than intertidal ones. That study, however. has compared different species, rather than subsets of the same, so that differences due to habitat cannot be distinguished from habitat-independent genotypic ones. Differences in respiratory rates between different popu- lations of a single species can be attributed in part to short term and long term acclimation to local temperature regimes. Studies on temperature acclimation have been done for many animals, with different species showing different patterns of response. Little work has been done on acclimation in poychaetes. Magnum (1972) has shown that intertidal onuphids do not acclimate, and Gladfeller (198) reports that the cirratulid, Cirriformia Diane Campbell, Temperature and habitat effects in Dodecaceria fewkesi. p. 3 spirabrancha acclimates to 7°0. This study was undertaken to compare both physiologically, but with emphasis on respiration, and morphologically, D. fewkesi from various habitats. The following characteristics were looked at: 1. Morphology and size of the animals, the pattern of tube construction, and mineral composition of the tubes. 2. Heat stress tolerance. 3. Respiratory rate / temperature curves and the 9 values for these. 4. Acclimation to experimental temperature regimes as measured by res¬ piratory rate. MATERTALS and METHODS General Descriptions: Portions of Dodecaceria fewkesi colonies were removed with hammer and chisel from three locations: Rocks between the O and 11.0 foot tide levels at the east end of Agassiz beach at Hopkins Marine Station (HMS), -10 feet on a piling below Wharf Two in Monterey, and at about -65 feet on the reef-like area seaward from HMS. Wet body weight was determined for groups of 5 animals each for 11 groups of intertidal worms, 14 groups of wharf ones, and 4 groups of deep reef ones. Numbers of tentacles were counted for 8 intertidal, 11 wharf, and 10 deep reef worms. Whether the vast majority of tubes was vertical or irregular in direction was noted for each colony. The maximun extension of newly growing tubes above the level of the rest of the tube mass was measured as well. Sex was determined by penetrating the integument with a dissecting needle and watching for release of gametes under a dissecting scope. Diane Campbell, Temperature and habitat effects in Dodecaceria fewkesi. p. 4 Tube composition: Percent magnesium in the tube material was determined by dissolving washed, dried, and powdered samples in dilute HCl, and precipitating out all alkaline earths except magnesium by the addition of ammonium carbonate solution. The filtrate was then assayed for magnesium by the method of Skoog and West (1965). Controls of known MgCo/CaCo were also run to determine the accuracy level of the test. Respiration: Colony samples, each seventy-five ml and containing about 40 to 200 animals, from the intertidal and the wharf were maintained at 6° - 2', 0 f 1.5°, and 20?C - 3°C in finger, bowls of seawater. Colonies to be kept at 20 were eae partitioned between two finger bowls to reduce fouling; in the other temperatures each entire colony was kept together. Additional animals were moved back and forth from 6% to 20' every day except Sunday. The water was changed at least once a day except for on two Sundays. For each temperature regime 120 intertidal worms were also removed from their natural tubes and placed in closed end holes drilled in plexiglass 1.27 cm deep and 0.23 cm in diameter, so that both their heads and hind ends extended out the open ends as they do under natural field conditions. Both number of deaths and the amount of skin pigment released when animals were transferred to room temperature seawater were noted after one and two weeks. Respiratory rates were measured for each group either one or two days after they were brought to the lab and placed in 12' running seawater, and after both one and two weeks in the various temperature regimes. The Warburg constant volume method was used to measure rates at 6.1', 12.0, Diane Campbell, Temperature and habitat effects in Dodecaceria fewkesi. p. 5 and 19.0°C - O.1°C. Animals were removed from their tubes with chisel and hammer, dropped on filter paper for about 30 seconds until excess moisture was gone before weighing, and placed in Warburg vessels containing artificial seawater isotonic with local seawater. Gasior (1976) showed that respiratory rates of D. fewkesi removed from their tubes and in their natural tubes were no different. Four or five replicate vessels were run for each experiment with five animals per vessel. Respiratory rates were measured at 30 minute intervals for two hours at each temperature with a two hour adjustment period in between. This adjustment period was found to be sufficient for the animals to reach a new stable respiratory rate. Each experimental run was started between 7:30 and 9:30 A.M. Res¬ piratory rates of one additional group of intertidal animals obtained from the field 4 weeks later were determined at 6.1 12.0°, 19.0°, and 25.0°c. The temperature was returned to 6.1°C over a period of 4 hours and the rate was remeasured. RESULTS There is no positive evidence for temperature acclimation over a two week period in animals from either the wharf or the intertidal. No respiratory rate / temperature curve measured after two weeks for any one group of animals is significantly different from the pre-acclimation one for animals from the same habitat, with the exception that intertidal animals maintained at 6°0 in their natural tubes for two weeks increased their respiratory rates. This increase is significant according to the Student t-test (p(0.05) when measured at 6.1° and 19.0°C. (Figure 1 and table 1 for intertidal animals; figure 2 and table 2 for wharf Diane Campbell, Temperature and habitat effects in Dodecaceria fewkesi. p. 6 animals.) However, both variation in weight between animals and any weight changes over the two week period must be taken into account. Wharf worms kept at 20° or cycled from 6° to 20°C lost about 5%% of their weight. When respiratory rates are recalculated assuming all weight change was due to water loss, the differences between pre-acclimation and post-accli¬ mation lines are more than compensated for. Intertidal worms kept at 6 were considerably smaller than the pre-acclimation sample. That no weight loss occurred is indicated by the facts that,contrary to wharf worms, for intertidal ones this is the only smaller group, this group alone was taken from the sparsely populated edge of a colony, and animals kept at 6° in plexiglass are as heavy as the pre-acclimation sample. In addition wharf animals which lost weight showed tightly drawn skin and loss of pigment and died soon after, whereas intertidal ones kept at 6' appeared healthy. Since these animals were then probably smaller to start with, and smaller animals generally have higher respiratory rates, their respiratory rates were adjusted to the average pre-acclimation weight according to the expression R - (W./W)'-bR,, where W,- average weight of an animal kept at 6°, W - average weight of pre-acclimation animals, R. - measured respiratory rate, and the coefficient b - 0.64, that of the closest relative for which it has been determined, Cirratulus cirratus, as measured by Courtney (1958). The corrected rate / temperature curve was still higher than that for pre-acclimation animals, but the difference, as for the case when it is corrected according to the other possible assumption for the cause of weight difference, was no longer significant. In addition, the rate / temperature curve for animals kept at 6° in plexiglass was not significantly higher than the pre-acclimation curve. Animals from the three habitats react differently to heat stress. Diane Campbell, Temperature and habitat effects in Dodecaceria fewkesi. p. 7 When kept in an incubator at 34 to 35°C, 20% of the deep reef worms died after two hours and 40 minutes, 20% of the wharf ones died after six hours, and after eight hours no intertidal animals had succumbed. At 37°0 20% of the deep reef worms died after two hours, and after about five hours 60% of the deep reef worms, 53% of the wharf worms, and no intertidal ones had died. No difference in death rates between animals that had been kept at different acclimation temperatures was readily apparent. Various temperatures produced many less severe effects in the worms as well. At 6°C D. fewkesi did not extent its tentacles fully, but no deaths occurred, at 12' it extended them fully and moved them slowly, and when kept at 20° for several days nearly all the animals moved out of their natural tubes and showed increased tentacle movement. Nearly all wharf animals kept at 20 % died after 1.5 to 2 weeks. When placed on filter paper for a few seconds and then put in seawater at room temperature, healthy wharf, but not intertidal, animals released a greenish yellow pigment through their skin which turned dark blue or black and precipitated after a few hours. Wharf worms put in 12' seawater put out no pigment. The temperature in which the animals were maintained influenced the amount of pigment released when put in room temperature water after two weeks. (Table 3) The 00 values calculated for the temperature range 12° to 19' are higher than those for the range 6.1 to 12° for animals from all three habitats for which respiratory rates have been measured one or two days after they were collected. This difference is significant at the p « 0.07 level according to the Student t-test for deep reef and intertidal animals. If data from experimental runs for all groups of worms from a given habitat, regardless of acclimation temperature, is pooled, this Diane Campbell, Temperature and habitat effects in Dodecaceria fewkesi. p. 8 difference is significant for animals from all three habitats. (p «0.01) (Table 4) The o for the one group of intertidal worms tested at 25° was 4.32 f 2.30 at 19.° to 25°, higher than 3.61 + 1.34 found at 12° to 19°, but not sig- nificantly so. When these animals were returned to 6.1° from 25°, their new respiratory rate was not significantly different from the rate obtained at 6.1° for all intertidal groups. The respiratory rate / temperature curves appear fairly similar for animals from all three habitats, although the rates of subtidal animals are slightly higher. Only data from animals freshly collected or main- tained in running seawater at 120 was included in the calculations. The difference is significant only when measured at 12°. (Student t-test. p (0.01) The respiratory rates were corrected for weight relative to each other according to the expression (w./w)-br., in which W - average weight of animals from all three habitats. When corrected, the rates of both subtidal populations were significantly higher than the rates of the intertidal one at all three temperatures measured. (All p (0.01) The wharf and deep reef rates were not significantly different at any temper- ature. (Figure 3) External as well as physiological differences for wharf and deep reef versus intertidal animals were found. Wharf and deep reef animals weigh considerably more than intertidal ones, have more tentacles, and extend their individual tubes farther above the mass surface level of the "worm rock". (Table 5) This agrees with results of a study by Kauhaner (1976) in which larger sample sizes were used. Wharf and deep reef worms also produce tubes protruding in many directions to form a cluster and live throughout the calcareous rock, whereas intertidal ones secrete tubes mostly in parallel with the openings pointing straight up and live Diane Campbell, Temperature and habitat effects in Dodecaceria fewkesi. p. 9 only near the top. Tube samples from both the intertidal and deep reef contain less than 1% magnesium. Kauhanen (1976) has shown that these animals do secrete their own tubes with an extension to artificial tubes noticeable after about three weeks. DISCUSSION Intertidal Dodecaceria'ability to survive extreme heat stress seems adaptive. Bolin and Abbott (1963) state that the average temperature difference between surface waters and the -65 foot level is only about two degrees during the spring. However, they indicate that the difference in maximum temperatures is about four degrees; the difference in maximum temperatures Dodecaceria from differing colonies is exposed to is pro¬ bably much greater, as the intertidal colony studied is exposed to am¬ bient air and sunlight at most low tides. Thus it makes adaptive sense that intertidal animals can cope with heat stress better than the subtidal ones. Wharf animals appeared to cope slightly better than deep reef ones at extreme high temperatures, which is consistent with the expectation that wharf ones are acclimatized to a temperature range a few degrees higher. Temperature stress increases the release of a pigment which Dales (1959) has shown to be a carotenoid stored in cells in the skin. This suggests that heat alters the permeability properties of the cell mem- branes in the skin. However, since the water in finger bowls with colonies at 20° became foul and presumably concommitantly lower in 0, tension, particularly for wharf animals, any changer in pigment, weight, and Diane Campbell, Temperature and habitat effects in Dodecaceria fewkesi. p. 70 respiratory rates could all be due to 0, as well as temperature stress. That no group of animals acclimated to a noticeable degree over a two week period seems adaptive when their mode of life and habitat are considered. D. fewkesi is a sedentary poychaete and spends its entire life in one location's temperature regime. Temperature at the wharf lo- cation probably changes little and slowly with the seasons, so that if wharf animals acclimate to any noticeable extent they probably do so over a longer period and only within a smaller temperature range. The intertidal animals cope with as large of a temperature range daily as they were subjected to in the lab. Hence it might be non-adaptive for them to acclimate in their physiological processes by synthesizing new isozymes so that reaction rates are substantially changed. The possibility that they acclimated to a slight degree beyond the accuracy of the measur- ment techniques used remains. The 9., was found to increase with temperature in D. fewkesi, whereas for basal metabolism in most animals it either decreases or remains constant, Precht (1973). Noted along with this increase in 0 was an increase in tentacle movement at higher temperature, so that these rate / temperature curves are probably for active metabolism. This is supported by Coyer and Magnum's (1973) work in which they found an in- crease in 9,, with temperature for active metabolism but not basal me- tabolism in Diopatra cuprea. They also found this uncommon phenomena of increasing 90 with temperature in Amphitrite ornata, another poly- chaete, for active and resting metabolism over small temperature ranges. D. fewkesi's rate curve indicates it is very sensitive to temperature changes in the range it normally lives in. The adaptive significance Diane Campbell, Temperature and habitat effects in Dodecaceria fewkesi. p. 17 of this is unknown. The larger subtidal animals tested showed similar although slightly higher rates than the intertidal ones. Most species show the opposite trend, a decreasing rate with increasing size, Prosser (1973). Therefore, either the respiratory rate of D. fewkesi is not influenced by size, or the subtidal animals have higher weight specific metabolic rates. When a weight correction factor is introduced, the difference between subtidal and intertidal animals is greatly amplified. The difference could be due either to adaptation to different temperature regimes or to a genetic difference between clones not necessarily correlated with habitat. Harrold (1976) arguesthat in the marine gastropod, Crepidula adunca, the minimum environmental temperature is of primary importance in setting respiratory rates, while Heath (1963) states that some fish respond to the upper ex- treme of the thermoperiod. Both the average maximum and the amount of change in temperature differ between subtidal and intertidal locations, so the animals could have adapted to different temperature regimes. It is also possible that the larger number of tentacles present in subtidal races may compensate partly for the usual decrease in respiratory rate with size. Gladfeller (1968) suggests this as an explanation as to why respiratory rates fall little with size in Cirriformia spirabrancha. Data on additional clones is needed to differentiate among the explanations given. That physiological differences between animals from various habitats, such as in respiratory rate, may exist is supported by other differences seen between the clones from different environments. The multi-directional arrangement of the subtidal colonies may be due to water circulating in all directions in the subtidal locations. Vertical tubes in the intertidal Diane Campbell, Temperature and habitat effects in Dodecaceria fewkesi. p. 12 would allow water to remain in them when the tide goes out. Tubes from the intertidal have shorter extensions than ones from the two subtidal locations, perhaps because forceful wave action wears down this relatively fragile structure. One similarity found between intertidal and deep reef tubes was their lack or near lack of magnesium. This, however, could certainly be controlled by different factors than the other character- istics are. Lowenstam (1954) found that magnesium concentration correlates with decreasing environmental temperature, with species with more than 85% aragonite (the mineral form with less than 1% magnesium) confined to the tropics. This trend was not followed in some habitats, and D. fewl appears to provide one of many exceptions to it. SUMMARY 1. Tube morphology, tentacle number, and body size varies between animals from various habitats. Magnesium content of the tubes is constant. 2. Over the range 6.1° to 19°0, the 90 for respiratory rates of D. fewkesi increases with increasing temperature. 3. The intertidal animals tolerate heat stress better than deep reef and wharf animals, as is indicated both by higher survival rates and by lesser amounts of carotenoid skin pigment released. 4. No positive evidence for acclimation in either wharf or intertidal animals to 6°,12°,20°C, or a variable temperature regime over a two week period was obtained. 5. Respiratory rate / temperature curves for the larger subtidal animals are fairly similar or slightly higher than that for intertidal ones. Diane Campbell, Temperature and habitat effects in Dodecaceri ja fewkesi. p. 1 This was interpreted to mean that subtidal animals have a higher effective rate than intertidal ones. Temperature and habitat effects in eri wkesi. D. Campbell ACKNOWLEDGMENT I wish to thank Dr. Robin Burnett for his unlimited support, en- couragement, and patience. p. 14 Diane Campbell, Temperature and habitat effects in Dodecaceria fewkesi. p. 15 REFERENCES Berkeley, E. and C. Berkeley. 1954. Notes on the life-history of the poychaete Dodecaceria fewkesi. J. Fish Res. Bd. Canada 11 (3): 326-334 Bolin, R.L. and D.P. Abbott. 1963. Studies on the marine climate and phytoplankton of the central coast area of California, 1954 - 1960. California Cooperative Oceanic Fisheries Investigations Courtney, W.A.M. 1958. Certain aspects of the biology of cirratulid poychaetes. PhD dissertation, University of London Coyer, P.E. and C.P. Magnum. 1973. Effect of temperature on active and resting metabolism in polychaetes. in Effects of Temperature in Ecto¬ thermic Organisms. Wieser, W, Ed. Springer-Verlag N.Y. Dales, R.P. 1963. Pigments in the skins of the polychaetes Arenicola, Abarenicola, Dodecaceria, and Halla. Comp. Biochem. Physiol. 8: 99-108 Gasior, B. 1976. Respiratory rates in Dodecaceria fewkesi under different experimental conditions. (Unpublished MS on file at Hopkins Marine Station library) Gladfeller, E. 1968. Certain aspects of the respiration rate of the rriformia spirabrancha. (Unpublished MS on cirratulid poychaete, C. file at Hopkins Marine Station library) Harrold, C. 1976. The effect of habitat and acclimation temperature upon the respiratory rate of the marine gastropod Crepidula adunca. In press Heath, W.G. 1963. Thermoperiodism in sea-run cutthroat trout. Science 142: 486-488 Kauhanen, G. 1976. Comparative studies of colonial morphology and the effects of selected environmental stresses on spatially separated Dodecaceria fewkesi. (Unpublished MS on file at Hopkins Marine Station library) Diane Campbell, Temperature and habitat effects in Dodecaceria fewkesi. p. 16 Lowenstam, H.A. 1954. Environmental relations of modification compo¬ sitions of certain carbonate secreting marine invertebrates. Proc. Natl. Acad. Sci. U.S. 40: 39-48 Magnum, C.P. 1972. Temperature sensitivity of metabolism in offshore and intertidal onuphid polychaetes. Marine Biology 17: 108-114 Precht, H, J. Christophersen, H. Hensel, and W. Larcher. 1973. Temperature and Life. Springer-Verlag N.Y. Prosser, C. L . 1973. Comparative Animal Physiology. 314 edition. W.B. Saunders Co. Philadelphia Skoog, D.A. and D.M. West. 1965. Analytical Chemistry. Holt, Rinehart and Winston, Inc. U.S.A. p. 17 Temperature and habitat effects in Dodecaceria fewkesi. D. Campbell Figure 1. Respiratory rate / temperature curves of intertidal animals. Respiratory rate is calculated as ul 0, consumed per gram wet weight per hour. Error bars were omitted for clearer comparison of curves. + Animals from the field o Animals kept at 12°0 for two weeks □ Animals kept at 6'0 for two weeks in their natural tubes. ....Respiratory rates corrected for weight for animals kept at 6°0 for two weeks —-—-Animals kept at 6°C for two weeks in plexiglass tubes • Animals kept at 20 C for two weeks Animals cycled between 6 and 20 Cfor two weeks Temperature and habitat effects in Dodecaceria 20 —e 15 20 Temperature c) 80 ewkesi. p. 18 190 Temperature and habitat effects in Dodecaceria fewkesi. D. Campbell TABLE 1 INTERTIDAL ANIMALS Respiratory rates (ul O, consumed/g/hr) Fest temperatures 19.00c 12.0°c 6.100 X 8 IX x X X 4 82.0 7.3 5 33.6 3.7 Freshly collected 5 24.9 5.5 4 42.0 13.6 3 117.2 24.5 3 51.9 20.5 Acclimated at 6°0 in natural tubes 4 38.2 12.4 3 47.2 18.7 3 106.7 22.3 Corrected for weight 4 26.1 10.1 3 42.4 4.6 4 80.9 4.9 In plexiglass tubes 5 32.9 4.1 5 90.5 23.4 5 30.5 10.8 Acclimated at 12°0 5 42.1 8.8 5 87.4 20.7 Acclimated at 19°0 5 26.3 10.1 4 37.2 10.6 4 87.2 17.6 Acclimated under a 4 30.6 10.2 variable temperature scheme TABLE 2 WHARF ANIMALS Respiration rates (ul O, consumedg/hi lest temperatures 19.000 6.100 12.000 n x nXS n x 8 + 30.3 5.4 4 43.4 2.7 5 98.1 23.5 Freshly collected 4 35.2 3.8 4 103.2 40.0 4 55.0 15.7 Acclimated at 6°0 5 84.7 20.7 5 40.3 9.2 Acclimated at 12°0 5 28.5 4.6 2 54.5 5.8 2 121.3 22.6 Acclimated at 19°0 2 39.0 9.7 Acclimated under a 4 115.3 30.4 3 51.5 22.3 4 34.3 12.2 variable temperature sch p. 19 Dodecaceria fewkesi. Temperature and habitat effects in Figure 2. Respiratory rate / temperature curves of wharf animals. Respiratory rate is calculated as ul 0, consumed per, gram wet weight per nour. Error bars were omitted for clearer comparison of curves. + Animals from the field o Animals kept at 12°0 for two weeks E Animals kept at 6 C for two weeks • Animals kept at 20 C for two weeks Animals cycled between 6 and 20°C for two weeks p. 20 20 Temperature and habitat effects in Dodecaceris D. Campbell 80 120 Temperature ewkes 0 190 p. 2 Temperature and habitat effects in Dodecaceria fewkesi p. 22 D. Campbell able 3. Amount of pigment released by animals when exposed to air followed by room temperature seawater. No pigment + Trace of pigment ++ Pigment made a yellow solution and precipitated out as black granules over a period of a few hours. +++ Water was opaque black after a few hours. — Temperature and habitat effects in Dodecaceria fewkesi. Amount of Pigmert released Acclimat ion TIME Temperature Intertidal Wharf O +++ 2 weeks 60 + 12° 2 weeks ++ + ++ 2 weeks 20 +++ 2 weeks 6°-20 — p. 23 + Temperature and habitat effects in Dodecaceria fewkesi. D. Campbell C O (O 0 X 8 O O IX IX O L — O) p.24 Temperature and habitat effects in Dodecaceria fewkesi. D. Campbell gure 3. Respiratory rate / temperature curves of animals collected fresh from the field or maintained in running 12°C seawater. Error bars were omitted for clearer comparison of curves. + Deep reef animals • Wharf animals Intertidal animals o Wharf animals for which the rates were corrected for weight E Intertidal animals for which the rates were corrected for weight p. 25 O 20 1.5 1.C 6.0 Temperature and habitat effects in Dodecaceria fewkesi. D. Campbell 12.0 Temperature (°) 19.0 p. 26 84 20 — V 5 a O+ 0OD O— 10 - OT - . O+ - o 0 8 5 Oa 8 0 O+ V 8 O — OC 90