ABSTRACT California sea mussels (Mytilus californianus) of 2 to 5 cm length were collected from intertidal areas in Pacific Grove, California, during May. They were placed in various dilutions of primary unchlorinated sewage and their respiration was measured. Results indicate that sewage causes changes in respiratory activity, and that high concentrations are extremely toxic. An attempt was made to isolate the toxic factors but proved unsuccessful. Data for the excretion of dissolved inorganic phosphate by the mussels are also presented. INTRODUCTION The city of Pacific Grove, California (population approximately 15,000) disposes household wastes in the intertidal area of Point Pinos. The outfall discharges wastes at an average rate of 1.6 million gallons per day. The sewage undergoes primary treatment and is chlorinated prior to discharge, but the detectable level of free chlorine in the water decreases rapidly within a few feet of the outfall. One of the irregularities in the intertidal community in the vicinity of the outfall which is in contrast to adjacent intertidal areas is the absence of the California sea mussel, Mytilus californianus (Conrad, 1837). Fifty feet northwest of the outfall, large M. californianus beds begin and continue up the side of the point. These locations are relatively unpolluted since the areas are washed by heavy surf at high tide, exposed to the air at low tide, are in waters which test low in excess nutrients and chemical pollutants, and have surface currents which keep the sewage out of the area. Southeast of these beds, in a direction toward the outfall, the intertidal rocks are barren of all life. But rocks in close approximation to the outfall and in a southernly direction down the point are densely covered with clusters of the barnacle Pollicipes polymerous. In uncontaminated intertidal areas, Pollicipes and Mytilus individuals often grow in the same area, or in adjacent clusters. Close macroscopic examination of the Pollicipes communities on the rocks in polluted areas showed no more than three to five Mytilus individuals per 15-20 Pollicipes clusters (each cluster with 20 - 30 individuals). None of the californianus were larger than 3.5 cm in length. Further south 70. down the point the population of M. californianus increased with occasional small clusters of 7-10 animals. Thus there seemed to be a gradient of density of M. californianus on the coastline southeast of the outfall, absence of any individuals at the outfall, and a large proliferation northwest of the pipe in relatively uncontaminated waters. The feeding habits of M. californianus suggest its susceptibility to any effects of sewage pollution. Fox (1936) stresses the great importance of finely divided organic debris or detritus that constitutes a large part of the material ingested by mussels and other lammellibranchs. He states that M, californianus normally feeds almost exclusively on detritus and the smaller planktonic organisms, and although mollusks have organs specialized for dealing only with small particles, selection of food is entirely nonqualitative. Anything which is not too large or spiny is ingested, although it may not be digested. Later, Fox (194- again notes that although M. californianus eats dinoflagellates, diatoms and bacteria, the largest fraction of its nutrituve material is detritus. It is assumed that organic material is ingested in a finely divided or partly colloidal state-not as dissoived organic matter. Thus M. californianus is a scavenger, which feeds largely on the types of materials which are likely to be found in sewage. If sewage has an effect on intertidal animals, it is likely that M. californianus is extremely susceptible. Tests were made on the acute toxicity and on the less severe metabolic stresses of primary unchlorinated sewage on M. californianus. Acute toxicity is scored by the death of an individual, or by the severe incapacitation of an individual's normal activity of byssus thread formation. To determine less severe stresses on metabolic activity, changes in respiration of individuals in various concentrations of sewage were measured. Acute toxicity was demonstrated with extremely high amounts of sewage, and respiration seems to be affected at lesser concentrations. However, conclusions from respiratory rate data are not well substantiated. In addition to these studies on the toxicity of sewage, two less intensive studies were conducted: 1) changes in the level of dissolved inorganic phosphates in the environment of the experimental animals, and 2) a preliminary investigation into the effects of the amines and amino acids in sewage on M. californianus. The level of dissolved inorganic phosphates in the sewage was used as a characterization of the amount of pollutants present. The level of phosphates in the solutions was higher after 24 hour contact with the mussels. Concerning the amines and amino acids, Fox (1936) states that a turbid sea water suspension of marine bacterial organisms, maintained by the addition of Witte's peptone, proved injurious to mussels: valves were kept tightly closed or death occurred if left immersed too long. He believes that the nitrogenous bacterial metabolites which are characteristic of decomposing protein matter caused the deleterious effects on the mussels. Fox cites Harvey (1925) as showing that with the copepod Calanus, bacterial growth supported by peptone is far more toxic than when supported by sugar. I extracted the amines and amino acids from a dilution of sewage twice as great as shown to be damaging, and subjected experimental animals to them. There was no acute toxicity demonstrated-no deaths nor absence of byssus thread formation. 64 METHODS AND MATERIALS For the study on respiratory effects in sewage dilutions, two experiments were conducted. The first experiment was carried out by mixing primary unchlorinated sewage from the Monterey treatment plant with sea water—the salinity was different in each of the separate dilutions of sewage. The second experiment was the same, except salinity differences were resolved by making the solutions isotonic with intertidal sea water. This was accomplished by adding 3.35 gm of sea salts to every 100 ml of sewage. Both experiments had the same array of M, californianus: five individuals in each of six jars. Each jar contained 750 ml of fluid: a control with 0% sewage, and jars with 0.5% sewage, 1% sewage, 2% sewage, 10% sewage and 50% sewage. Each jar had five Mytilus with approximately corresponding lengths of 5 cm, 4 cm, 4-3 cm, 3 cm, and 2 cm, (Table 1). The 30 individuals in the experiment with differing sewage concentrations were collected at Hopkins Marine Station. The solutions in the jars were changed daily, temperature was maintained at that of sea water, the jars were kept in a room with dim lighting, and were aerated by vigorously bubbling air through glass tubes at the top of the jars, just below the water line. Respiration tests were conducted by placing an individual in a ground glass-stoppered bottle filled with a measured amount of fresh sea water, and incubating the bottles in a small aquarium under the same conditions of temperature (sea water) and light (dim) for 3 hours. At the end of the incubation period, the amount of dissolved Oo left in the sea water was determined according to the Winkler method as described in Strickland and Parsons (1968). This value was then subtracted from the amount of Op initially present in the sea water. The amount initially present was determined by incubating several known volumes of sea water without Mytilus in the jars, and averaging the values. The amount of 02 left in the bottle was calculated according to the following equations: 360 ml 0/liter - Va - R. st- R 2 50 2 V5-2 where Vg - volume of thiosulfate titrated (ml) Rb = reagent blank (ml) Vst" standardization titration (ml) Vb - volume of bottle (ml) In this equation, 50 ml aliquots are used for the titration. m1 02 - m1 0g/liter x V, (in liters) Respiration is expressed in ml 0/hr/gm wet weight; the mussel was removed from the valves and weighed without its byssus threads. The experiment with variable sewage and salinity was conducted for a period of 4 weeks. The experiment with only variable sewage concentrations lasted five days. Due to deaths in the 50% sewage concentration, I prepared another jar of five Mytilus (lengths of 5.1 cm, 4.0 cm, 3.6 cm, 3.0 cm, and 2.0 cn), of 506 sea water and 506 tap water to observe byssus thread formation and deaths. To characterize the amount of dissolved inorganic phosphates in the jars, 100 ml aliquots were sampled and analyzed according to the procedure of Murphy and Riley (1962), using the Klett electrophotometer. To test deaths and byssus thread formation in an environment of amines and amino acids present in sewage, the following extraction procedure was used with 800 ml of primary unchlorinated sewage from Monterey: Oe raise pä to 10 with Naon extract three times with 240 ml aliquots of diethyl ether extract the ether fraction three times with 240 ml aliquots of O.1 M HCI 4) evaporate the aqueous fraction to dryness dissolve the dry residue with 800 ml sea water The solution was characterized by titrating a 50 ml sample with 0.1M HOl and O.1 M NaoH, measuring pH as the dependent variable. The remaining 750 ml were put into a jar with two Mytilus (lengths of 4.4 om.and 2.9 cm) and a control jar was set up with 750 ml sea water and two Mytilus (lengths of 4.5 cm and 3.0 cm). These animals were kept under the same conditions as all the other experimental animals. Observations were recorded concerning byssus thread formation and death. RESULTS Acute toxicity. In jars with sewage and salinity dilutions, acute toxicity occured in the 50% dilution. (Table 2). After two days in the 50% sewage:salinity environment, none of the mussels formed byssus threads. By the tenth day one was dead, and by the thirteenth day, all had died. From the sixth to thirteenth day, the mussels indicated a moribund condition by showing sluggishness in closing their valves when the mantle edge was prodded with forceps. In the jar with 50%-sea water: 50% tap water, the mussels did not form byssus threads for the first two days, but by the third day three out of five were connected to the jar. By the twelfth day, the mussels byssus thread formation was normal. They continued to function normally for the remaining eight days of the experiment. In the jars with various sewage concentrations, acute toxicity was observed in the 50% dilution. The valves remained closed for the entire four days, and there was no byssus thread formation by any of the animals. No deaths were observed in 50% sewage over the course of the experiment. To determine if amines and/or amino acids in the sewage were toxic, two mussels were placed in a jar with 750 ml of sea water containing amines and amino acids extracted from 750 ml of primary unchlorinated sewage. The characterization titration with 0.1 M NaOH and 0.1 M HOI did not detect the presence of any amines and detected only one amino acid (pk approx. 6.1) in the 50 mi sample. (Figure 1). Two control animals were placed in 750 ml of uncontaminated sea water. These animals were observed for 11 days, and no acute toxicity was evident. Normal byssus thread formation was present in all four animals from the first day onward. Since the solutions in the two jars were not changed, byssus thread formation became erratic towards the end of the 11 day observation period, but irregularities occured in both the control and experimental animals. Respiration. The respiration of 30 mussels in jars of sewage and salinity dilutions was measured from three to five times and the values then averaged. The 30 averages representing the respiration of the 30 individuals were graphed as ml 0/hr/gm wet weight. (Table 3 and Figure . In the 50% dilution of sewage and salinity, in which all the animals eventually died, respiration was lower than the control values in four out of the five test animals. It was approximately 30% lower for the 5 cm mussel, 274 lower for the 4 cm mussel, 20% lower for the 3 cm mussel, and 35% lower for the 2 cm individual. In the 1% dilution of sewage and salinity, respiration increased fromethe control value in four out of five test animals. It increased approximately 294 for the 4 cm mussel, 23% for the 3-3.5 cm mussel, 10% for the 3 cm mussel (up to 17% in the 2% dilution), and 18% for the 2 cm individual. The respiration of the 30 mussels in the jars of sewage dilutions with sea water salinity was measured two to three times and the values averaged (Table 4 and Figure 3). In the 50% dilution of sewage, respiration was higher than the control values in four of the five individuals. It was approximately 17 higher for the 5 cm mussel, 48% higher for the 3.5-4 cm mussel, 32% for the 3 cm mussel, and 28% for the 2 cm mussel. In the 0.5% dilution of sewage, four of the five individuals respired less than control, but the decrease is not very large for the 5 cm and 4 cm mussels. Phosphate levels. The changes in the phosphate levels in the six jars of the sewage:salinity dilutions, the 50% tap water:50% sea water jar, and a jar of 10% sewage without mussels were measured over a 24 hour period. (Table 5). The amount of dissolved inorganic phosphate increased in all the jars except in the 50% tap water: 50% sea water. The increases in the control, 0.5%, 1%, and 2% dilutions are roughly equivalent; the 10% dilution increase is larger. No readings were made on the 50% dilution. The level of phosphates also rose in a jar of 10% sewage without any test animals in the solution. DISCUSSION The experiments on acute toxicity indicate that primary unchlorinated sewage is toxic to Mytilus californianus if present at high levels in the environment. In other toxicity studies conducted by my colleagues with primary sewage from Pacific Grove, (chlorinated and unchlorinated), proved to be even more injurious to intertidal test animals than primary unchlorinated effluent from Monterey. Thus it is possible that the paucity of M, californianus on the rocks covered with Pollicipes polymerous southeast of the Point Pinos outfall is due to sewage pollution of that area. Although acute toxicity was demonstrated only at 50g concentrations in my work, observations were made for only a two-week period, and the sewage I used was not from Foint Pinos. The data on the respiration of the California sea mussels in deleterious environments are not conclusive; more tests should have been performed. However, examination of the data in Tables 3 and 4 shows that in a large number of cases, the figures for onygen consumption of each mussel were gery similar. Moreover, when the data is graphed, (Figures 2 and 3), it shows variation of respiratory activity with age. This concurs with experiments on Nytilus perna by Bayne (1967), and adds credibility to my work. The respiration graphs show several interesting trends. In Figure 2 where the 50% dilution proved lethal, respiration of the moribund mussels was substantially lower than the controls. Figure 3 (variable sewage and constant salinity) shows the opposite trend for the mussels in the 50% dilution; this indicates a different response to an environment where salinity is not a factor. I believe that the mussels show respiration values higher than control values because they were making up an oxygen debt during incubation which was acquired while in the sewage. This hypothesis is supported by several facts. Fox (1936) has shown that chemotactic responses are demonstrated by M. californianus for certain substances. The mussel remains with its valves shut tight in such hostile 1 10- environments. In a series of experiments with M, californianus in various concentrations of sea water, Fox (1936) noted that in water of salinity below 14.94 %/00 the mussels either remained with valves closed, or opened only after many hours and then reclosed permanently. Both of these observations suggest that my mussels could detect a hostile sewage environment and responded by isolating themselves from it. The hypothesis is further supported by two observations I made in the lab. During the respiration test incubation, I noticed that a few of the individuals from the 50% sewage dilution had fixed themselves to the bottles with byssus threads. This happened only occasionally with any of the mussels, including the control animals. Perhaps the mussel detected a favorable change in the environment and began functioning to make up for its decreased activity in the sewage. Also, the turbidity of the 50% sewage dilution decreased very little in the 24 hours it was in contact with the experimental animals. This is in contrast to my observations on the other sewage dilutions and the sewage:salinity dilutions. It is also inconsistent with the fact that Mytilus is known to be very effective in lowering the turbidity of murky waters in a matter of hours (Fox, 1936). In summary, I believe that the mussels could not survive in the 50% sewage dilution, and when placed in a healthy environment, they attempted to make up an oxygen debt acquired during incubation. The changes in respiration demonstrated at 1% sewage:salinity and 1% sewage dilutions indicate that the respiratory activity of M. californianus is extremely sensitive to small changes in the environment. The meaning of the changes in respiration at 10 dilutions is not clear; they may be an indication of increased feeding activity due to a solution slightly richer in detritus than the control, or may be a reflection of osmotic stress in a less than normal salinity. The data on dissolved inorganic phosphate levels serve the practical purpose of roughly characterizing the sewage from Monterey used in the experiments. The results also suggest an hypothesis concerning phosphate excretion in M, californianus. The values for the control animals, the 0.5%, 1%, and 24 sewage:salinity dilutions indicate that the mussels increased the level of phosphate by about 20 Klett units in 24 hours- approximately 0.07 ugm-at/1 (an increase of 0.053 ugm-at in these 750 ml jars). The mussels in the 10% dilution increased the environmental level of phosphate by a measure of 10 Klett units,more, but this can be accounted for by the fact that sewage under the same conditions but without mussels increased in phosphate by 5-10 Klett units in the same period. ERENCE Bayne, B.L. 1967. The respiratory response of lytilus perna L. (Mollusca: Lamellibranchia) to reduced environmental oxygen. Physiological Zoology 40 (3): 307-313. Fox, D. L., G. W. Marks, F.0. Austin. 1936. The survival period of adult mussels in sea water of various concentrations. In Fox, D. L. (ed.). The Habitat and Food of the California Sea Mussel. California University Scripps Institution of Oceanography Bulletin 4: 1-10. Fox, D.L. 1936. Certain physical and chemical properties of the fecal pellets and some experimental feeding studies. In Fox, D.L. (ed.). The Habitat and Food of the California Sea Mussel. California University Scripps Instiution of Oceanography Bulletin 4: 49-60. Fox, D.L. 1943. Biology of the California sea mussel (Nytilus californianus) II. Nutrition, metabolism, growth and calcium deposition. Journal of Experimental Zoology 93: 205-249. ACKNONLEDGEMENTS I would like to acknowledge the help given me by Dr. John Phillips in my amine extraction work, and for his valuable criticisms of project. also thank my advisor, Dr. Ellsworth Wheeler, for his patience and encouragement throughout the quarter. My work was supported in part by the National Science Foundation Undergraduate Research Program, grant no. GY-7288. TABLE LEGENDS Table 1. Measurements of length and weight of each of the 60 mussels used in the respiration experiments. Note that there are 5 in each dilution of sewage:salinity, and 5 in each dilution of sewage. Table 2. Data on acute toxicity-byssus thread formation and death used as criteria. Empty squares indicate normal functioning, X's indicate absence of byssus threads in all five animals, and blacked-out squares indicate that all five are dead. 2b, 3b,4b, indicate the number of mussels with byssus threads (short of all 5), and 10, 30 show the number dead (short of all 5). Table 3. Raw data from the sewage:salinity experiment, expressed in ml 02/3 hrs, used to graph the respiration curves. in Figure 2. Table 4. Raw data from the sewage experiment, expressed in mi 0,/3 hrs used to graph the respiration curves in Figure 3. Table 5. Phosphate readings measured in Klett units. Measurements were taken in the 50% salinity jar, the jars of sewage: salinity dilutions, and a jar of 10% sewage: salinity with no mussels in it. SEWAGE ANL -N SALINTT VARIABLE SEWAGE VARIABLE 5.2 cm 38 gm 4.2 1.98 5.5 1.84 3.2 0.87 2.0 D.21 5.2 cm 3.27 gm 2.05 6 1.48 2.0 0.3 5.2 cm 2.69 gm 4.2 2.00 91 3.2 cm 5.1 gm 3.37 4.0 2.21 1.06 3.0 0.84 2.2 % DILUTION 5.4 cm 5.3 cm 5.2 cm 3.50 gm 3.13 gm 2.97 gm 1.59 2.71 3.4 3.6 1.24 1.16 1.2. 3.2 3.2 0.8 O.81 2.2 0.42 0.22 4.8 cm 5.3 cm 5.0 cm 3.52 gm 3.64 gm 3.07 3.9 1.67 1.50 2.14 3.8 3.4 3.5 1.38 1.07 1.51 3.0 3.C 2.9 1.05 O.78 2.0 2.1 O.40 0. 5.3 cm 4.00 gm 2.04 1.67 1.23 2.2 0.48 4.9 cm 3.52 gm 1.97 3.6 1.00 3.1 O.8 O.31 e 155 ee 1r — 155 e — 15 — 15 E e e 125 L LL — e5 able 117 cm 4 cm -3.5 cm 3 cm 2 cm 54684 .72720 3470 70380 49900 39662 39250 .57962 .48412 47012 48919 50654 5820 .32976 .27464 .09217 .11648 .13424 % SEWAGE: SALINITY 0.5 54694 .45092 .52504 64989 .67946 .60210 54885 .71134 49036 3892 44562 51727 48874 .47588 .47038 .50841 54838 44024 43030 50504 41823 .50484 48620 .46791 50724 165 34452 .22894 36960 .20042 33513 .19662 .21788 .18850 .13624 .14770 .08976 .10010 .14391 13810 .38604 .60021 .60360 57336 62625 .63862 2552 6. .60850 4059. 33425 143 5774 122 42714 54969 39599 2442 20683 .12402 .1476 .51038 57840 .65462 233 .6 34281 3855 34656 35464 46033 14661 34853 57843 44447 34650 .28784 28590 25116 .18915 .14742 .17991 50 .50604 .65475 .47156 46354 5762 44940 .273 .2. .64116 49212 238 58538 .41605 16485 .27825 .08672 .27664 .10686 .16038 .08258 Le cm 4 cm 3.5-4 cm cm 2 cm .70830 5832 55863 51926 34375 40378 4305 738 34645 16544 .15400 % SEWAGE .64638 .65105 65554 .62314 437 55010 .57465 48169 34426 .50427 34761 49734 27326 30589 .23530 .27131 .12025 .10912 .0999 .09698 .74601 .71914 .28675 37802 30400 .31642 35139 34047 14616 .18244 .741 .7893 .58050 .55160 360 .43848 34541 .21138 .27562 .19810 .17976 .83510 84280 .63825 57200 .40225 .50427 49 544 46384 .47866 .19117 410 4 TAP:g SEA 0% DILUTION O.5% DILUTION 1% DILUTION 27 DILUTION 10% DILUTION 50% DILUTION 10% DILUTION WITH NO MUSSELS: initial value 10,25 3, 10, 10 15, 20, 15 20, 30, 35, 35, 45. 150, 165, 160, 190 no data 150, 165 increase after 24 hrs -7.0 15, 30, 15 15, 20, 10 5, 20, 2 55, 20, 20, 30 35, 10, 30, 25 5, 10 FIGURE LEGEND Figure 1. The titration curve used to characterize the amine/amino acid extraction. A 50 ml aliquot of the 800 ml total extractionwas titrated. Figure 2. The respiration curves for the 30 mussels in sewage:salinity dilutions. The % SEWAGE:SALINITY axis is distorted between the 10% and The approximate 50% dilution in order to make the graph more compact. lengths of the mussels are noted above their curves. Figure 3. The respiration curves for the 30 mussels in sewage dilutions with the salinity made up to equal control. The % SEWAGE axis in distorted between the 10% and 50% dilution in order to make the graph more compact. The approximate lengths of the mussels are noted above their curves. p + 2 41 2 5 2 m 0peEhr- pergm 82 Tr 2 — a2 r S en m1 05 perhE per en e im Figun 3 k2