Lipid and Glycogen Levels in the Tissues of Two West Coast Chitons; Mopalia muscosa and Nuttallina californica ABSTRACT Analysis was done on the foot, gut, digestive gland, and gonad using the methanol-ethyl ether method for lipids and the phenol-sulfuric acid method for glycogen. Species differences were found only in the foot tissues. Female Mopalia muscosa (Gould, 1846) had a lower percentage of lipid in the foot tissue than did female Nuttallina- californica (Reeve, 1847). Comparing both sexes, N. muscosa was found to have a higher level of glycogen in the foot tissuethan N. californica. In the tissues of both species studied lipids are quantitatively the more important storage materials. Original paper containing full findings is in library of Hopkins Marine Station. Robert Tenold Hopkins Marine Station Pacific Grove, Calif. 93950 R. Tenold Storage Reserves In Two Chitons Page 1 Introduction Of the several species of Polyplacophora found in the intertidal area of Monterey County California, Nuttallina californica (Reeve, 1847) and Mopalia muscosa (Gould, 1846) are two of the most common. The habitat, behavior, and food of these two species differ greatly. Nuttallina californica is a small chiton, usually no longer than 3.7 cm which is usually restricted to the middle intertidal of fairly exposed rocky shores (Ricketts & Calvin, 1962). They are often found in small furrows and crevices in the rocks and appear to lead a rather sedentary life. From personal observation some have been found not to move at all during a 48 hour period. They have been found to feed mostly on red algae in their immediate vicinity. These include Endocladia muricata, Gigartina papillata, and Rhodoglossum spp. They are also known to feed on the green alga Cladophora trichotoma (Nishi, 1974). Mopalia muscosa is the larger of the two species and is in the size range of 7.6-10.2 cm. They are found in more protected areas such as; tidepools, attached to the underside of rocks, or on top of rocks under a covering of Pelvetia fastigiata or Fucus furcatus (Legard & Andrus, 1974). Their activity is more pronounced than that of R. Tenold Storage Reserves In Two Chitons Page 2 Nuttallina californica. They have been found to show much activity during the hours of high tide, occurring during the night (Smith, 1974). Boolootian (1951) found them to feed on various red and green algae such as; Gelidium spp., Ulva spp., and Ectocarpus spp. The impetus for this comparative study of lipid and carbohydrate stores was a test of the following hypothesis; differences in habit and habitat are reflected in the levels of tissue lipid and glycogen. Using movement as an indication of active feeding it was hypoth- esized that the more sedentary Nuttallina californica, which has prolonged periods of inactivity, may have higher or lower lipid and carbohydrate stores than those of Mopalia muscosa, which seems to move and feed more fre- quently. Materials & Methods Nuttallina californica of relatively the same size were collected from similar habitats at Mussel Point near the Hopkins Marine Station, in Pacific Grove and at Point Pinos on the Monterey Peninsula. Mopalia muscosa were collected from Mission Point in Carmel Bay. Animals were collected during the last week of April and the month of May, 1974. Immediately after collection the animals were R. Tenold Storage Reserves In Two Chitons Page 3 brought into the laboratory, weighed and then dissected to obtain the foot, gut, digestive gland, and gonad. The gut was extended in a dissecting pan and a bent dissecting probe was run the length of it squeezing out the contents to insure that only the gut tissue was analyzed. The tissues were then placed in separate crucibles and dried in an oven at 75 degrees centigrade for 24 hours. Upon completion of drying the tissues were kept in a desiccator until the analysis could be made. Dried foot tissue was ground into a fine powder using a mortar and pestle and the other tissues were broken into fine pieces using a dissecting probe and the end of a small test tube. Lipids were extracted using the methanol-ethyl ether method of Freeman, Lindgren, Ng, and Nichols (1957). After the lipids had been extracted from the tissue it was digested in 10 ml of hot 10% trichloroacetic acid for 30 minutes. The supernatant was then analyzed for carbohydrate content using the phenol-sulfuric acid method of Dubois, Giles, Hamilton, Rebers and Smith (1956) with reference to a glucose standard curve. Therefore, all carbohydrate levels are expressed in terms of glucose. The entire organ of each animal was used for analysis. Therefore, percent of tissue dry weight is also percent of organ dry weight. c 6 Storage Reserves In Two Chitons Page 4 R. Tenold Results & Discussion Ten organisms from each species, five of each sex, were analyzed. The results of lipid and carbohydrate levels for female Mopalia muscosa are shown in Table 1, male M. muscosa are shown in Table 2, female Nuttallina californica are shown in Table 3, and male N. californ¬ ica are shown in Table 4. The mean level of carbohydrates for both species, standard error for each tissue and the range between individuals are shown in Figure 1. Figure 2 shows the same information for lipid levels in both species. The findings show a great variability in lipid and carbohydrate levels between individual organisms within each species. It has been shown by Giese and Araki (1962) that the chemical composition of tissues does change depending on what stage of the reproductive cycle the animal is in. This study was only conducted over a five week period and individuals analyzed were of differing gonadal developement. Dry weights of the gonad from each individual were recorded but there was no apparent relationship between gonadal size and tissue storage levels. In answering the original hypothesis the only significant difference found between the two species in terms of lipid stores was in that of the foot tissue of the females of both species. Using the t-test this R. Tenold Storage Reserves In Two Chitons Page 5 difference was found to be significant to the 97.5% confidence limit. Mean lipid content of the foot of female Nuttallina california was 8.7% of the dry weight of the tissue. This is to be compared to a value of 4.5% for the same tissue in the female Mopalia muscosa. This finding would tend to confirm the original hypothesis however no significant difference could be found between any of the other tissues. Looking at the carbohydrate levels the only significant difference between the two species was found in the foot tissue of both sexes. These findings were subjected to a two-tailed t-test and were found to surpass the 99% confidence limit. The mean value for carbohydrates in the foot of female and male Mopalia muscosa was 7.0% and 4.3% respectively. These levels are to be compared to 1.6% and 1.7% for female and male Nuttallina californica. These findings show the foot tissue of M.muscosa as a prominent storage site for carbohydrates as compared to the other tissues in both species. It is to be remembered that M. muscosa is a far more active animal than N. californica. The findings also showed intraspecies differences between females and males concerning lipid and carbohy¬ drate content of the gonads. Lipid content of the ovary was much higher than that of the testis, probably reflecting R. Tenold Storage Reserves In Two Chitons Page 6 the large amount of storage reserves deposited in the eggs to be used in developement. In Mopalia muscosa the level of carbohydrates is significantly higher at the 95% confidence limit level in the testis than it is in the ovary. The possible reason for this difference is not apparent. However when the tissues are corrected for their difference in lipid content there is not a significant difference between the carbohydrate levels of the ovary and testis. The results of the "t-test for significant difference between mean values is presented in Tables 5 and 6. As in other species of Polyplacophora studied; Katharina tunicata, Cryptochiton stelleri (Giese, 1969) and Mopalia hindsii (Giese & Araki, 1962) Mopalia muscosa and Nuttallina californica seem to have most of their storage reserves in the form of lipids, and their carbohydrate stores are much lower. This trend probably indicates a fast overturning carbohydrate reserve used for immediate energy and a more stable lipid reserve drawn on for the production of gametes and in periods of starvation. Summary 1. Lipid and carbohydrate levels were determined in the foot, gut, gonad, and digestive gland of two Page 7 R. Tenold Storage Reserves In Two Chitons Monterey Bay chitons, Nuttallina californica (Reeve, 1847) and Mopalia muscosa (Gould, 1846). A difference between species in storage reserves of 2. lipids and carbohydrates due to an observed difference in activity and feeding frequency was investigated. The foot tissue was found to be different between species in terms of lipids and carbohydrates. Other tissues were not significantly different. 4. Lipids are quantitatively the more important storage materials. The levels of these two storage substances was 5. found to be extremely variable from organism to organism in both species studied. Storage Reserves In Two Chitons Page 8 R. Tenold Acknowledgments I would like to thank Dr. John H. Phillips for his timely advice concerning this project and for his assistance in writing this paper. I also wish to thank Dr. Robin Burnett for his help with the statistical analysis of data. My sincere thanks also go to Rich Williams for the use of his chiton restrainer. I also would like to thank all of the faculty and personnel of Hopkins Marine Station and especially my fellow students for making Biology 175H an unforgettable experience. R. Tenold Storage Reserves In Two Chitons Page 9 Literature Cited Boolootian, R. A. 1964 On growth, feeding and reproduction in the chiton Mopalia muscosa of Santa Monica Bay. Wessenschaften Meeresuntersuchen 11: 186-199 Dubois, Michel; Giles, K.A.; Hamilton, J.K.; Rebers, P.A.; Smith, Fred 1956 Colorimetric method for determination of sugars and related substances. Anal. Chem. 28: 350 Freeman, N.K.; Lindgren, F.T.; Ng, Y.C.; Nichols, A.V. 1957 Serum lipid analyses by chromatography and infrared spectrophotometry. J. Biol. Chem. 227: 449-464 Giese, Arthur Charles 1969 A new approach to the biochemical composition of the Mollusc body. Oceanogr. Mar. Biol. Ann. Rev. 7: 175-225 Giese, Arthur Charles & Araki, George 1962 Chemical changes with reproductive activity of the chitons, Katharina tunicata and Mopalia Storage Reserves In Two Chitons R. Tenold Literature Cited (cont.) hindsii. J. exp. Zool. 151: 259-267 Legard, William & Andrus, Jon 1974 Personal Communication. Nishi, Rae 1974 Personal communication. Ricketts, Edward F. & Calvin, Jack 1962 Between Pacific Tides. Stanford Univ. Press; xii + 516 pp. Smith, Suanne 1974 Personal communication. Page 10 R. Tenold Storage Reserves In Two Chitons Figure Captions Figure 1 Carbohydrate levels in the digestive gland, gut, gonad, and foot of both sexes of Nuttallina californica and Mopalia muscosa are shown. Horizontal lines show mean carbohydrate levels expressed in per cent of dry tissue weight. Shaded areas show standard error for each sample analyzed and arrows show the range of levels found within each sample analyzed. Sample size was five in all cases. Figure 2 Lipid levels in the digestive gland, gut, gonad, and foot of both sexes of Nuttallina californica and Mopalia muscosa are shown. Horizontal lines show mean lipid levels expressed in per cent of dry tissue weight. Shaded areas show standard error for each sample analyzed and arrows show the range of levels found within each sample analyzed. Sample size was five in all cases. 2 8 10 3 8 2 8 Digestive Gland Mopalia raad Nattallina Gonad Gut muscosa Figare 1 californica + + 8 Foot 8 30 20 /0 O 50 10 S 30 20 10 + Digestive Gland Digestie Gland Gat Gut Figure 2 califorica Vattallina Gonad Foot Mopalia muscosa + 8 Foot Gonad R. Tenold Storage Reserves In Two Chitons Table Captions Table 1 Lipid and carbohydrate levels, expressed in per- cent of dry tissue weight are shown for the digestive gland, gut, gonad, and foot of five female Mopalia muscosa analyzed. Mean values are also shown. Wet body weight and dried gonad weight for each animal are also given; body weight is expressed in grams and gonad weight is expressed in milligrams. Table 2 Lipid and carbohydrate levels, expressed in percent of dry tissue weight are shown for the digestve gland, gut, gonad, and foot of five male Mopalia muscosa analyzed. Mean values are also shown. Wet body weight and dried gonad weight for each animal are also given; body weight is expressed in grams and gonad weight is expressed in milligrams. Table 3 Lipid and carbohydrate levels, expressed in percent of dry tissue weight are shown for the digestive gland, gut, gonad, and foot of five female Nuttallina california analyzed. Mean values are also shown. Wet body weight and dried gonad weight for each animal are R. Tenold Storage reserves In Two Chitons Table Captions (cont.) also given; body weight is expressed in grams and gonad weight is expressed in milligrams. N.R. means weights were not recorded. Table 4 Lipid and carbohydrate levels, expressed in percent of dry tissue weight are shown for the digest- ive gland, gut, gonad, and foot of five male Nuttallina californica analyzed. Mean values are also shown. Wet body weight and dried gonad weight for each animal are also given; body weight is expressed in grams and gonad weight is expressed in milligrams. Table 5 Data from comparison of lipid content of tissues using the t-test is shown. The table shows tissues from the two types of chitons being compared, also the sample size n, mean value,X, of each tissue; standard deviation, S.D., of each tissue; the t value arrived at and the probability, p, of the two tissues being significantly different. Table 6 Data from comparison of carbohydrate content of tissues using the t-test is shown. The table shows R. Tenold Storage Reserves In Two Chitons tissues from the two types of chitons being compared; also the sample size, n; mean value, X, of each tissue; value standard deviation, S.D., of each tissue; the t arrived at and the probability, p, of the two tissues being significantly different. Table 1 Chiton 17.30 18.92 18.98 24.09 32.27 grams Weight Gonad 210.3 242.0 152.6 198.8 223.6 milligrams Weight Lipid Content Mean Digestive 50.28 9.0 9.2% 7.4% 5.0% 16.2% Gland 15.8 Gut 24.0 13.3 12.4 8.6 20.6 Gonad 20.8 19.9 20.7 20.6 15.6 19.5 Foot 6.2 4.0 5.2 4.4 4.5 2.7 Carbohydrate Content Digestive 2.6 % 4.8% 1.1% 1.0% 3.5% 2.8% Gland Gut 4.0 4.2 1.6 2.7 1.8 2.9 Gonad 2.7 3.4 2.3 1.2 2.8 2.5 Foot 8.4 9.6 8.8 4.7 3.4 7.0 Table 2 Chiton 26.16 22.92 36.40 31.16 24.13 grams Weight Gonad 271.5 245.9 252.1 277.8 247.8 milligrams Weight Lipid Content Mean Digestive 7.0% 8.3% 9.8% 11.9% 8.1% 9.0% Gland Gut 13.0 12.0 20.2 13.7 14.6 14.7 Gonad 7.8 8.8 9.6 9.1 9.7 9.0 Foot 4.1 5.2 4.6 9.8 4.5 5.6 Carbohydrate Content Digestive 3.7% 3.2% 4.3% 2.1% 3.2% 2.5% Gland 4.0 4.0 Gut 3.5 3.0 2.3 3.4 4.8 4.4 Gonad 4.4 1.8 4.1 5.3 Foot 4.4 3.6 4.3 6.0 2.2 5.2 0 Table 3 Chiton N.R. N.R. 8.15 4.72 6.32 grams Weight Gonad N.R. N.R. 41.04 65.75 25.16 milligrams Weight Lipid Content Mean Digestive 12.8% 3.8% 6.6% 12.5% 31.49 13.4% Gland Gut 18.8 16.2 13.1 16.7 32.3 19.4 Gonad 15.0 21.8 15.3 22.4 23.0 19.5 Foot 7.4 12.6 6.4 5.6 11.6 8.7 Carbohydrate Content Digestive 2.3% 3.1% 3.1% 2.1% 2.6 % 2.5% Gland 4.5 3.2 Gut 2.4 2.6 2.5 3.0 Gonad 3.9 2.0 2.8 2.0 2.6 2.6 Foot 1.4 1.8 1.6 1.9 1.7 1.4 Table 4 Chiton 4.94 4.45 6.95 9.40 4.16 grams Weight Gonad 22.02 28.89 3.43 119.16 34.33 milligrams Weight Mean Lipid Content Digestive 7.3% 6.6% 4.4% 7.9% 7.6% 10.1% Gland 13.4 Gut 7.2 7.5 13.3 21.8 17.2 11.9 15.3 9.3 8.7 9.8 11.0 Gonad Foot 8.3 5.1 11.8 9.9 9.1 5.7 Carbohydrate Content Digestive 2.1% 1.4% 2.6 % 1.3% 3.7% 1.6% Gland 4.9 Gut 3.8 2.7 5.3 2.9 3.9 Gonad 3.2 3.1 3.3 2.4 3.8 3.2 Foot 1.6 1.7 2.0 1.6 1.6 1.8 Table 5 Chitons issue Compared A. Digestive Gland A. Female B. Digestive Gland Nuttallina californica A. Gut B. Gut Female A. Gonad Mopalia muscosa B. Gonad A. Foot B. Foot A. Digestive Gland B. Digestive A. Male Gland Nuttallina californice A. Gut B. Gut B. Male Mopalia A. Gonad muscosa B. Gonad A. Foot B. Foot A. Digestive Gland B. Digestive A. Female Gland Nuttallina A. Gut californica B. Gut B. Male Nuttallina Gonad californica B. Gonad A. Foot B. Foot X S.D. P ts 5 13.4 10.76 .279 —- 16.2 19.10 7.44 19.4 32 -830 — 15.8 3.99 19.5 2.22 010 -- 19.5 8. 3.17 2.76 97.5 4.5 1.72 7.3 2.07 1.36 --- 9.0 1.89 13.4 6.29 .411 —- 14.7 3.22 2.69 11.0 1.60 --- 0.76 9.0 2.85 8.3 2.34 1.62 —- 5.6 5 13.4 10.76 1.24 --- 2.07 7.3 19.4 7.44 6.29 1.37 -- 5 13.4 3.90 19.5 11.0 2.69 3.95 99.5 3.17 8.7 8.3 2.85 0.21 -- Chitons Compared A. Female M. muscosa B. Male M. muscosa Table 5 (cont.) Tissue S.D. t P A. Digestive 16.2 19.10 Gland O.83 -- B. Digestive 9.0 1.89 Gland A. Gut 15.8 6.3 O.34 -- B. Gut 14.7 3.22 19.5 A. Gonad 2.22 10.11 99.9 B. Gonad 9.0 0.76 4.5 A. Foot 1.72 0.95 --- 5.6 2.34 B. Foot Table 6 Chitons issue Compared A. Digestive Gland B. Digestive A. Female Gland Nuttallina california Gut Gut Female B. Mopalia Gonad muscosa Gonad B. A. Foot B. Foot Digestive Gland Digestive A. Male Gland californica A. Gut B. Gut B. Male A. Gonad muscosa B. Gonad A. Foot B. Foot A. Digestive Gland B. Digestive A. Female Gland californica A. Gut B. Gut B. Male A. Gonad californica B. Gonad A. Foot B. Foot 2.6 2.6 3.0 2.9 2.7 2.5 1.6 7.0 2.1 3.2 3.9 3.4 3.2 4.1 1.7 4.3 2.6 2.1 3.0 3.9 2.7 3.2 1.6 1.7 S.D. S .460 .026 — 1.61 .873 1.20 :240 — .779 .357 ——— .816 O.23 4.33 99.5 2.74 1.02 ——— 1.72 O.89 1.16 ——— 1.73 0.72 O.50 1.36 1.61 -- 0.18 3.87 99.5 1.46 O.46 1.00 -- 1.02 O.87 ——— 1.16 1.35 0.78 1.40 -- O.50 0.23 0.62 -- O.18 Chitons Compared A. Female muscosa B. Male muscosa Table 6 (cont.) Tissue A. Digestive g Gland B. Digestive Gland A. Gut B. Gut A. Gonad B. Gonad A. Foot B. Foot S.D. 2.6 1.61 0.89 3.2 2.9 1.20 3.4 0.72 2.5 0.82 4.1 1.36 2.74 7.0 4.3 1.46 t P O.63 --- O.61 -- 2.34 95.0 1.94 --- + Tened 1 ++ — Tenolt 0 Figare dattalling caldernca * 4 ++ 3 0 6 Cond Pak Oigestrie 6ue Gland Mopala masosa /0 3 21 P a- Digestwe Gut Gonad Foot Gland —. 10 - Terdt . 30 15 /0 5 50 45 10 § 35 30 25 20 0 are 2. 6 Diaestwe laad 9 8 Ogestwe at Gland Nattallina caltorce 0 23 9 d Gut Gonad Foot Popala musese P S P foet Gonad Terde