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Effect of water temperature and food on energy allocation in the stalked barnacle, Pollicipes polymerus Sowerby
J. Exp. Mar. Biol. Ecol., 1983, Vol. 69, pp. 189-202
189
Elsevier
EFFECT OF WATER TEMPERATURE AND FOOD ON ENERGY ALLOCATION IN THE STALKED BARNACLE, POLLICIPES
POLYMERUS
Sowerby
H.M. PAGE Marine Science Institute, University of California Santa Barbara, Santa Barbara, CA 93106. U.S.A. Abstract:
The effects of water temperature and. food level on absorption efficiency, rate of oxygen consumption, molting rate, reproductive condition, energy content, and total production have been studied in the stalked barnacle, Pollicipespolymerus Sowerby. Absorption efficiency measured gravimetrically was high (~94%) and unaffected by water temperature or food level. Absorption efficiency measured using an ash-ratio method was substantially less than that determined gravimetrically. The rate of oxygen consumption increased in the high food treatments and decreased in the starved treatment after 40 days. Molting rate, energy content, and total production were highest in the high food treatments. Reproduction was inhibited at warm water temperatures. The greater influence of food level than water temperature on production is probably related to the thermal regime experienced by these animals in the field.
INTRODUCTION
Water temperature and food availability have been shown to influence the growth and/or reproduction of a variety of marine intertidal invertebrate species (see for example, Barnes, 1963; Sastry, 1975; Bayne, 1976; Hines, 1978). Few studies, however, have considered the influence of these variables on growth and reproduction in the context of the total energy budget of the organism. Those experimental studies available on energy partitioning of intertidal species have been confined largely to mollusks. For example, at water temperatures > 20 ’ C, the energy available for growth of laboratory maintained mussels, Mytilus edulis, decreased as a result of increased metabolic rate and reduced filtering rate (Thompson & Bayne, 1974; Bayne, 1976). Similiar results were obtained on M. californianus from San Juan Island, Washington, at water temperatures > 22 “C (Bayne et al., 1976). Assimilation efficiency and the fraction of ingested energy available for growth and reproduction is dependent on food level in M. edulis (Thompson & Bayne, 1974; Widdows, 1978; Riisgard & Randlov, 1981) and in M. californianus (Bayne et al., 1976; Elvin & Gonor, 1979). By measuring changes in energy budget components in the laboratory, the present study investigated the influence of water temperature and food level on absorption efficiency and food energy partitioning in an intertidal crustacean, the stalked cirriped, Pollicipespolymerus Sowerby. This barnacle is frequently found associated with Mytilus cal~fimiunus and iU. edulis on exposed rocky shores and pier pilings along the Pacific coast of North America. In the Santa Barbara area, Pollicipespolymerus can experience 0022-0981/83/$03.00 0 1983 Elsevier Science Publishers B.V.
I90
H.M.PAGE
water temperatures ranging from 12 “C in late winter to > 20 ‘C in . late summer (University of California, 1970-1980; Neushul, unpubl. data). Highest brooding frequencies of P. polymerus are in the winter (Straughan, 197 1; Page, in prep.). Reproduction of P. polyments collected 60 km north of Santa Barbara was inhibited at water temperatures of 20 “C in the laboratory (Cimberg, 1981).
MATERIAL
AND
METHODS
P. polymerus were collected
on small pieces of rock from the mid-intertidal ( + 0.75-1.0 m M.L.L.W.) at Goleta Point, Santa Barbara, a soft shale headland along a protected outer coast bordering the Pacific Ocean. Ambient water temperature at the time of collection was 15.5 “C. Groups of three to five individuals were cleaned of adhering material and fastened with rubber bands to plastic stands. Within 24 h of collection four groups of 50 individuals each (16.0 + 1.Omm capitulum height, hereafter designated ch, k SD) were placed in separate recirculating whirlpools (Fig. 1).
A
Fig. I. Diagram
of experimental apparatus: arrows indicate direction of water flow; A, water inflow from reservoir: B, screen; C, water outflow to reservoir.
Whirlpools were used in each treatment to provide the proper environment for feeding. P. polyments (except for very small individuals, Lewis, 198 1) depend on water flow to carry food particles to their extended cirri. Sea water was pumped from a temperature controlled 100-l reservoir into the whirlpool through small nozzles producing rapid water flow. Water circulated around the whirlpool and through a bottom
ENERGY
ALLOCATION
IN POLLICIPES
POLYMERUS
191
screen which caught uneaten food, feces, and exuviae. The barnacles were orientated with the feeding apparatus facing the water flow. Each group of 50 barnacles was subjected to one of four treatments: cold water (13.2 + 0.9 ‘C, + SD) with high or low food ration (designated CH and CL, respectively) or warm water (19.8 f 0.5 ‘C) with high or low food ration (WH and WL, respectively) for 40 days (30 May to 8 July) in ambient light conditions. These water temperatures are typical of those experienced by P. polymenrs in the late winter and late summer in Santa Barbara. A control group of 15 barnacles was placed in cold water (13 “C) and starved. Each day either two (low ration) or 12 (high ration) brine shrimp adults (Artemiu salina (L.), San Francisco) per individual barnacle were added to the whirlpools. Artemiu adults were used for food for the following reasons : (1) they are easily counted, (2) they are easily recovered if uneaten, (3) they remain homogeneously suspended in the water column, and (4) they are similiar to the crustacean diet of Policipes polymerus in the field (Barnes, 1959; Howard & Scott, 1959; Lewis, 1981; Page, in prep.). The experimental animals were exposed to ambient air temperature for x 10 min each day while feces, exuviae, and uneaten Artemiu were removed. They were also exposed to air for up to 1 h every 4 days while water in the reservoirs was replaced and brought to the desired temperature. Forty specimens of P. polymerus, collected from the same location and of the same size (16.0 f 1.0 mm ch) as the experimental animals were sacrificed at the beginning of the experiment to estimate the initial energy content of barnacles used in each treatment. Five samples of 300 Artemiu were taken during the course of the experiment, rinsed several times in de-ionized water to remove adhering salt, and dried to a constant weight at 60 ‘C to estimate individual dry weight. The soma and any egg masses in the mantle cavity of barnacles were removed, rinsed in de-ionized water, dried to a constant weight at 60 “C and weighed. The remainder of each barnacle was frozen, then thawed to permit easy separation of the sheath from the stalk. Ovaries, if present, were removed from the stalk and both were weighed after drying at 60 ‘C. P. polymerus produce compact feces and these were also gently rinsed prior to being dried and weighed. The caloric content of the soma and stalk tissues, ovaries, food, exuviae, and feces was determined using a Parr 1411 microbomb calorimeter. Dried samples were ground to a fine powder with a mortar and pestle and pelletized prior to combustion. Subsamples were ashed at 450 “C for 24 h to determine ash-free dry weight (AFDW). ABSORPTION
EFFICIENCY
Efficiency of absorption of the Artemia salina by Pollicipespolymencs in each treatment was determined gravimetrically using both the dry weight and caloric content of the food and feces: A = [(C - F)/C] x 100, where A is the absorption efficiency, C the dry weight or calories of food ingested, and F the dry weight or calories of feces egested. Absorption efficiency was also determined using the ash-ratio method of Conover
H. M. PAGE
192
(1966). This method, frequently employed where the quantitative recovery of feces is impractical, assumes that only the organic fraction of the food is absorbed. The following formula was used for the calculation of absorption efficiency by this method: U = (F - E)/( 1 - E)F, where U is the absorption efficiency, E the organic fraction in the food, and F the organic fraction in the feces. OXYGEN
CONSUMPTION
Measurements of rate of oxygen consumption, obtained using four groups of two to three individuals (16 mm ch) at the beginning, mid-point, and end of the experiment provided estimates of the metabolic rate of individuals in each treatment. The same animals were followed over time. A temperature-controlled flow-through respirometer (180-ml capacity) was used. An air stone in the reservoir maintained the water at air saturation. A small magnetic stirring bar enclosed in the respirometer facilitated mixing. The small pieces of shale rock on which the barnacles were attached were rinsed in de-ionized water to remove adhering microorganisms prior to each measurement. Antibiotics may influence barnacle behavior (Cimberg, 1978) and were not used. Outflowing water (flow rate = 2 ml. min- ‘) was collected in a stoppered 50-ml Erlenmeyer flask. At the end of an experiment (6 h duration) the oxygen in samples of water flowing into the flask was determined by microburette titration (Winkler, from Strickland & Parsons, 1968). Oxygen consumed was the difference in oxygen concentrations between water flowing into and out of the respirometer multiplied by the flow rate. Respiration experiments were done in darkness. Controls without animals were run at both temperatures and did not exceed 10% of the oxygen consumed. This was taken into account when calculating respiratory rates.
RESULTS
ABSORPTION
EFFICIENCY
The number and dry weight of Artemia salina ingested by Poiiicipes polymer-us and the number of calories ingested and egested is given in Table I. The caloric content of the Artemia was 4747 k 46 cd. g dry wt.- ‘. Individuals in the high ration treatments ingested approximately five times as many calories as those in the low ration treatments. Absorption of ingested food measured using gravimetric techniques was unaffected by experimental water temperatures or ration and ranged from 93 to 95yj0 (Table I). The ash-ratio method greatly under-estimated absorption efficiency of Pollicipes polymerus producing values of from 26 to 41 “/b (Table I). The relatively small increase in the percentage of ash in the feces (16-19%) compared with that in the food (127;) indicates a high (= 90 ‘&) absorption of inorganic material (Table I). No data are available on the excretory losses of soluble materials. The excretory loss of other species feeding carnivorously is generally < 10% absorbed energy (Brett & Groves, 1979).
ENERGY
IN POLLICIPES
ALLOCATION
TABLE
Summary
193
POLYMERCJS
I
ofnumber, dry weight, and calories ingested as Artemiu salina and dry weight and calories egested as feces by Pollicipes polymerus in each treatment: for key to treatments see p. 191. Treatment
Initial no. barnacles Final no. barnacles Ration (no. Artemiu. ind- ’ . day- ‘) Aver. no. Artemia ingested. ind- ’ . day- ’ Total no. Artemiu ingested. ind-’ treatmentDry wt. Artemia ingested. ind- ’ (mg) Calories ingested. ind-’ Feces dry wt. ind- ’ (mg) Feces caloric content (Cal. gg ‘) Cal. egestedind- ’ Cal. absorbed. ind- ’ (ingested-egested) (A) Absorption efficiency (%) Dry weight Calories Ash-ratio Ash absorption (T,,)
BODY WEIGHT
AND CALORIC
’
CH
CL
WH
WL
50 50 12 8.9 356 126 598 7.7 4518 34.8 563
50 45 2 1.9 76 30 142 2.2 4493 9.9 132
50 46 12 9.2 368 129 611 6.7 4934 33.1 578
50 50 2 1.7 68 23 109 1.1 4476 5.1 104
93.9 94.2 37.5 90.9
92.6 93.0 40.7 88.4
94.7 94.5 26.3 93.1
95.1 95.4 33.9 93.0
CONTENT
Only barnacles at the higher temperature and with a high food ration increased in total body tissue weight (P < 0.05, Student’s t-test) (Table II). Barnacles starved for 40 days decreased in total body weight (P < 0.05, Student’s t-test). At the low temperature and with a high ration the caloric content (cal *g dry vv- ‘) of both soma and stalk tissues increased (Table II). MOLTING
FREQUENCY
Molting frequency in each treatment was calculated as the average number of molts produced per day for each consecutive lo-day period (Fig. 2). Two-way analysis of variance was done on square-root transformed data (Sokal & Rohlf, 1969) over each lo-day interval. No effect of water temperature or ration on molting frequency was evident between 1 and 10 or 11 and 20 days. A significant interaction (P < 0.001) between temperature and ration was found between 21 and 30 days, whereas ration alone influenced molting frequency between 31 and 40 days (P < 0.001). Unlike most crustaceans, the exuviae of barnacles contain little calcium carbonate. The ash fraction of P. polymenu exuviae was 7.1% (N = 39) and the caloric content 4356 f 106 cal .g-‘. Multiplying the average weight of an exuvium (5.6 x 10e3 g) by its caloric content gave an estimate of 24.4 calories per exuvium. One molt represented a loss of 1.5-2.0x of the energy content of the combined soma and stalk tissues.
body ueight
different
(P) (Acal
* Significantly
Production
Exuviae
’)
from initial sample
ind(P < 0.05).
_
264+ 67 1093 + 359 21 1378
4708 4633
Energy content (Cal. ind-‘) Soma Stalk Ovaries and brood Total
gm’ i
18 20 + 6 4+7
’
(cal
56& 14 236 + 51 292 + 71
Reproductive condition 0x brooding good wt (mg dry wt) Ovary wt (mg dry wt)
Exuviae Aver. no. ind-
Caloric content Soma Stalk
repr~lducti\e
Initial
(k SD).caloric cuntcnl.
Body weight (mg dry wt) Soma Stalk Total
A\cragc
+ 109
21 -_--_
270 + 53 1145 + 359 51 1466
25 1955 10 * 5*
1.19
4819 4934
56j, 11 232 + 63 288 f 84
-48
13
241 f 59 1044 f 386 31 1317
17 14+ 8 6+4
0.77
4717 4881
51+ 13* 214 + 52 265 t 73
CL
and change in energ! treatment see p. 191.
CH
condition,
T~BI F II
+ 156
28
248 + 54 1253 f 360* 5 1506
0* 0 1 +2*
1.75
4684 4692
53 * 12 267 k 72* 320 + 60*
WH
(production)
Treatment
content
WL
III each treatment:
-48
21
210+ 73* 1094 f 430 5 1309
0* 0 1 + t*
1.20
4651 4655
45 + 16* 235 k 48 280 + 62
of barnacle>
_
-272
7
225 k 37* 870 + 198* 5 1099
0* 0 1+ _- 7*
0.47
4694 4620
48 f 8* 188+40* 236 k 35*
Starved
for key to
z
2
z
ENERGY ALLOCATION IN POLLZCZPZS Z’OLYMERLIS
l-10
11-20 TIME
21-30
195
31-40
(days]
Fig. 2. Molting frequency of barnacles in the fed treatments: average number of molts per day asker square-root transformation.
REPRODUCTION
There was a decline in the percentage of barnacles carrying egg masses in the warm water treatments after 40 days (P < 0.05, chi-square test) and the average weight of ovary also decreased (P -C0.05, Student’s c-test) (Table II). Neither high nor low food ration had a significant effect on reproduction at either water temperature. The percentage carrying egg masses (P -C0.05, chi-square test) and average weight of ovary (P < 0.05, Student’s t-test) did, however, decline during starvation. The caloric content of well-developed ovaries was 5128 f 15 cal *g dry wt-‘. The time of development ofP. polymerus embryos (25-30 days, Hilgard, 1960; Lewis, 1975) and the stage of development (early or intermediate) suggest that egg masses in the mantle cavity of barnacles in the cold water treatments were produced sometime during the 40-day period. ENERGY CONTENT
The energy content of the soma, stalk, ovaries, and egg masses of barnacles in the intial sample and in each experimental treatment was determined by multiplying tissue dry weight by the corresponding caloric content. These values, summed with the energy lost in the production of exuviae, were compared with the initial sample to estimate the “actual” change (sensu Riisgard & Randlov, 198 1) in individual energy content during the experiment (production, P, Table II). Ration, rather than water temperature, had the greatest influence on change in total energy content. Total energy content increased in the high ration treatments and decreased in the low ration and starved treatments. The increase in energy content of barnacles in WH was due primarily to an increase in weight. By contrast, an increase in caloric content and the production of ovarian tissue contributed to the increase in
IYh
H.M.
PAGE
energy content of barnacies in CH. The decrease in energy content of starved barnacles was due primarily to a 20% decrease in weight. OXYGEN
CONSUMPTION
The results of respiratory measurements on barnacles from each treatment at the beginning, mid-point, and end of the experiment are given in Table III. Because it was not possible to weigh accurately individual barnacles attached to small rocks and because of the possibility of body weight or compositional changes during the experiment, the results are expressed per ~di~du~ rather than per g weight. TABlk
111
Rate of oxygen consumption of barnacles in experimental treatments (see p. 191): the same ammals measured over time; average of four determinations + SD. Rate of oxygen consumption rreatment
(ml.
h- ’ ind ’ i
Day 0
Day 20
Day 40
CH CL.
0.074 + 0.009 0.073 + 0.009
0.079 i 0.024 0.073 * 0.019
0.127 * 0.027*
WH WI.
0.106 + 0.009 0.090 * 0.014
0.118 k 0.02P 0.08Y -t_0.027
0.134 + 0.007* 0.090 + 0.030
0.077 fr 0.00’)
0.074 -i: 0.007
0.059 + o.u07*
Starved * Signi~cantly
(13 “C) different
from Day 0 (P < 0.05, Student’s
were
fJ.064
2 0.1820
t-test).
At Day 0, the respiratory rate of barnacles in the warm water treatments was signif?cantly higher than those in cold water (Q10 = 1.57) (P < 0.05, Student’s t-test). With time, however, the respiratory rate of barnacles fed the high ration in both temperature treatments increased and was higher than those on low food after 40 days (P < 0.05, Student’s t-test). The respiratory rate of starved P. polyrnerus declined after 40 days (P < 0.05, Student’s t-test). To determine whether the increase in individual respiratory rate in the CH and WH treatments was due to an increase in body weight, an estimate of oxygen consumption per dry weight (ml . g dry wt- ’ . h.- ‘) at Day 40 was made (Table IV). Since barnacles were not weighed until the end of the experiment, the estimate of weight-specific respiratory rate for each treatment at Day 0 was made using the average dry weight of the initial sample. The weight-spec~c respiratory rate of well-fed barnacles increased independently of an increase in body weight. Two estimates of the fraction of absorbed energy expended in respiration are derived from the general energy budget equation A = R + P + E, where A is the absorbed energy (calories), R the energy used in resp~ation, and P the production measured as changes in energy content, including molt and ovary production (Table IV). The excretion of soluble materials (E) was not taken into account in these calculations.
ENERGY
ALLOCATION
IN POLLICIPES
POLYMERUS
197
The first estimate was obtained by subtracting production (P) (Table II) from absorbed calories (A) (Table I). This estimate assumed a balanced energy budget (R = A - P). In the second estimate, the amount of oxygen consumed by barnacles in each treatment, estimated separately for the first 20 days and the second 20 days from Table III, was multiplied by 4.8 cal . ml 0; ’ (Brody, 1945) to yield the calories expended in respiration (Table IV). This value was divided by absorbed calories (Table I) to calculate the respiratory fraction. TABLE IV Estimates
ofweight-specific respiratory rate, respiration fraction, and scope for growth for barnacles treatment (see p. 191): + , estimated using average body dry weight of initial sample.
CH
CL
WH
WL
in each
Starved
Oxygen consumption rate (ml O,.g dry wt-‘.h-‘) Day 0’ Day 40
0.24 0.44
0.23 0.24
0.34 0.42
0.32 0.32
0.24 0.25
Respiration fraction Estimate from production (1 -P/A)
0.81
1.36
0.73
1.46
_
Estimate from 0, consumption (R/A )
0.73
2.42
0.88
3.96
-
Estimated calories expended in respiration from 0, consumption measurements
411
319
509
412
314
Scope for growth
(A - R)
+ 152
-187
+69
-308
-314
Estimates of the respiratory fraction made from oxygen consumption data were appreciably higher than those determined from measuring production in the low ration treatments (Table IV). No consistent pattern was evident with water temperature. Estimated caloric losses in respiration (Table IV) alone were from 1.3 (respiration estimate) to 2.7 (production estimate) times greater in barnacles in the high ration than low ration treatments. SCOPE
FOR
GROWTH
The number of calories used in respiration (R) was subtracted from absorbed calories (A) to yield the “scope for growth”, (Warren & Davis, 1967), the “estimated” energy available (sensu Riisgard & Randlov, 1981) to barnacles in each treatment for growth and reproduction (Table IV). The high ration treatments, at both water temperatures had a positive scope for growth, indicating that energy was available for growth and reproduction. A negative scope was found for barnacles in the low ration and starved treatments, indicating that these barnacles were metabolizing their body tissues for
H.M. PAGE
19x
m~nt~n~ce. The scope for growth and the production estimates were in agreement on whether energy was gained or lost by barnacles during the experiment. The actual values differed, however, between these two estimates, particularly for the low ration treatments. MAINTENANCE
RATION
The maintenance ration of submerged P. polymerus (16 mm ch) was estimated using data on the scope for growth (Table IV) and the energy content decrease (Table II) of starved specimens. The oxygen consumed by starved barnacles converts, using 4.8 Cal. ml 0; ’ , to a maintenance energy expenditure of z 7.9 Cal. ind ’ . day ’ . The maintenance ration estimated from a decrease in body weight (P) is slightly lower; 6.8 Cal. ind- ’ . day- ’ (272 cal in 40 days). DISCUSSION
The absorption efficiency of P. po&merus feeding on Artemia salina was not affected by a five-fold difference in ration or a seven degree difference in water temperature. These results are consistent with the hypothesis that the absorption efkkiency of invertebrates feeding carnivorously is relatively inflexible, being influenced primarily by type of food (Lawton, 1970). By contrast, the absorption efficiency of herbivores and detritivores appears more flexible. For example, the absorption efficiency of ~yti~us edulis feeding on algae was inversely related to food level and perhaps water temperature (Thompson & Bayne, 1974; Bayne, 1976; Widdows, 1978). Absorption efficiency was inversely related to ingestion rate in the isopod, Armadillidium vulgare, (Hubbell et al., 1965) and the snails, Ancylus jluviatilis and Planorbis contortus, (Glow. 1975). Absorption efficiency for two other barnacle species fed Artemia salina nauplii exceeded 90ya : Balanus improvisus (94%) (Kuznetsova, 1973) and Balanus glanduIa (99%) (Wu & Levings, 1978). Absorption efficiency of Pollicipespolymerus was under-estimated when determined by the ash-ratio method. Similiar results have also been noted for chaeto~aths (Cosper & Reeve, 1975), shrimp (Forster & Gabbott, 1971) and mysids (Lasenby & Langford, 1973). The under-estimate in the present study was due to the high assimilation of ash by P. po!vmerus. This indicates that food is a potentially important source of minerals for shell production in this species. Few data are available on the effect of food and water temperature on the molting frequency of P. polymerus or other temperate-water barnacles. The molting frequency of P. polymerus (16 mm ch) does not appear great. An estimate of intermolt interval can be obtained using the “instantaneous” method (Fusaro, 1978) over the first ten days of the experiment: f, = t/p,, where f,, is the intermolt interval in days, t the total number of days held (10 days), and pt the proportion of individuals which molted in t (10) days. The estimate of a 40-day intermolt exceeds values (generally < 7 days)
ENERGY ALLOCATIQNIN
~~LLZCZ~ESFOLY~E~WS
199
reported for other temperate-water barnacles (Costlow & Bookhout, 1953,1956; Davis et al., 1973 ; Losada, 1975). The weight loss and energy loss on molting appear small ( w 2.0% ), consistent with the estimation on ~~i~~~ g~~~~~~ of 2.3 % (Wu & Levings, 1978). The high molting rate of Pollicipespolymerus in WL between 2 1 and 30 days followed by the drop between 31 and 40 days, in comparison with the continued increase in WH suggests that warm water may accelerate molting and deplete energy reserves after 30 days. A similiar pattern, on a shorter time scale, was found for the boreo-arctic species, Balanus buhnoides (Pate1 & Crisp, 1960). Food level appeared most important and acted in combination with water temperature. The molting rate of fed B. baianoides increased linearly with water temperature from 3 to 20 “C. The increased molting rate at higher temperatures apparently, however, utilized food reserves more rapidly, resulting in a reduced rate when food was withheld (Pate1 & Crisp, 1960). The increase in respiratory rate of Pollicipes polymer-us on high ration was probably related to changes in the nutritional state of these barnacles. Seasonal changes in the oxygen cons~ption rate of Balanus bul~~ides was attributed, in part, to seasonal changes in the level of food supply (Barnes et al., 1963). Thompson & Bayne (1972) found an increased oxygen requirement resulting from the presence of food in the guts of Mytilus edulis. Davies (1967) correlated higher respiratory rates of limpets (Patella ~~g~t~) with high av~labi~ity of food and suggested higher respiratory rates may be associated with active somatic and reproductive growth. The influence of water temperature on the measured respiratory rate of freshly collected Pollicipes polymerus although significant, was small (Qlo = 1.57). No consistent influence of water temperature was found on the “actual” or “‘estimated” energy available for growth and reproduction. Although good agreement between the two estimates was obtained for the high ration and starved barnacles, the measured respiratory rate of individuals in the low ration treatments was higher than predicted from changes in energy content. These results are similiar to those obtained by Riisgard & Randlov (198 1) on Myths edulis and suggest that the low ration animals became more active during respiration experiments. The results of the respiratory studies on Pollicipespolymerus conducted by Barnes & Barnes (1959) cannot be compared directly with those of this study since they measured rates of the soma alone and their results are expressed per g *wet wt- ’ at 10 “C. A respiratory rate of 0.05 ml O2 * g- ’ +h- * for an animal of 200 mg wet weight from Barnes & Barnes (1959) converts to 0.25 ml 0, *g dry wt- ’ . h-’ (assuming the soma is 80% water; Page, unpubl. data) which agrees well with the values for the starved and low food animals measured at 13 “C at the end of the present experiment. The greater influence of food rather than environmental water temperature in influencing estimated and actual production for P. polymerus is not surprising given the intertidal existence of this organism. Fyhn et al. (1972) found the body tissue temperature of P. polymerus was equal to that of ambient sea water when submerged, but could increase during air exposure. Bvin & Gonor (1979) showed that the mussel, ~~fj~~~
X(1
H.M. PAGE
~~~z~~~j~~~~, also experiences short-term thermal shocks from exposure to air, coastal upwelling, and other factors. This mollusk, as well as M. edzdis,is capable of maintaining a relatively constant rate of oxygen consumption over a wide range of environmental water temperatures. Above certain critical water temperatures, however, the scope for growth declined as a result of a sharp increase in the energy devoted to metabolism. Critical water temperatures, which elicit a sharp increase in respiratory rate, appear to exceed 20 ‘C for Pollicipespolymerus from Santa Barbara. Water temperature strongly influenced the amount of absorbed energy partitioned to somatic and reproductive tissues in P. poIymerus. The implications of these results for field conditions are that, given a constant amount of food, there can be an energy “trade-off’ between reproduction and growth (or storage) regulated by water temperature.
ACKNOWLEDGEMENTS
I thank Drs. A. Wenner, A. Kuris, D. Morse, and J. Childress as well as S. Willason, T. Mickel, and P. Hiller-Adams for helpful comments on the manuscript. I also thank F. Dewitt and P. Siegel for technical assistance and J. Popp for drawing the apparatus. Funding was provided by the Marine Science Institute and a University of California Patent Fund grant. REFERENCES BARNES.H., 1959. Stomach contents and microfeeding of some common cirripedes. Can. J. ZooI., Vol. 37. pp. 231-236. BARNES.H., 1963. Light, temperature, and the breeding of Balanus balanoides. 1. Mur. Biol. Assuc. U.K., Vol. 43, pp. 7 1l-727. BARNES,H. & M. BARNES. 1959. Studies on the metabolism of cirripedes. The relation between body weight, oxygen uptake, and species habitat. Verofl Inst. ~eeres~rsch., Bremerhaven, Vol. 6, pp. 5 15-523. BARNES,H., M. BARNES& D.M. FINLAYSON,1963. The seasonai changes in body weight, biochemical composition, and oxygen uptake of two common boreo-artic cirripedes, Bahnus halanoides (L.) and Bultmus balanus (L.). J. Mar. Biol. ,4ssoc. U.K., Vol. 43, pp. 185-21 I.
BAYNE,B. L., 1976.Marine mwsels: their ecology andphysiologv. Cambridge Universtty. CambrIdge, 494 pp. BAYNE,B. L.. C.J. BAYNE,T. C. CAREFOOT& R. J. THOMPSON,1976. The physiological ecology of ~.vtiiu.s ca~z~rn~an~ Conrad. I. Metabolism and energy balance. Oecologia (Berlin), Vol. 22, pp. 211-228. BRETT.J. R. & T. D. D. GROVES, 1979. Physiological energetics. In, Fish physiologv, Vol. 8, edited by W. S. Hoar, D. J. Randall & J. R. Brett, Academic Press, New York, pp. 279-352. BRODY, S., 1945. Bioenergetics and growth. Reinhold, New York, 1023 pp. C.SLOW.P., 1975. The feeding strategies of two freshwater gastropods, Ancylusfluviatilis Mull. and Planorbis contorr~s Linn. (Pulm~ata), in terms of ingestion rates and absorption efficiencies. Oecofogiu (Berkn), Vol. 20, pp. 33-49. CIMBERO,R. L., 1978.Patterns and causes of reproductive activity in the barnacle Polficipespo&merus. Ph.D. dissertation, University of Southern California, Los Angeles, 119 pp. CIMBERG,R. L.. 1981. Variability in brooding activity in the stalked barnacle PoNicipespolymenrs. Biol. Bull. (Woods Hole, Mass.), Vol. 160, pp. 31-42. CONOVER, R.J.. 1966. Assimilation of organic matter by ~oopIankton. Limnof. Oceanogr., Vol. Il. pp. 338-345. COSPER, T.C. dlt M.R. REEVE.1975. Digestive et%ciency of the chaetognath Sagitta hispida Conant. J. E.up. Mar. Biol. Ecol.. Vol. I?. pp. 33-38.
ENERGY ALLOCATION IN POLLICIPES
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COSTLOW,J.D. dc C.G. BOOKHOUT,1953. Molting and growth in Balanus improvisus. Biol. Bull. (Woods Hole, Mass.), Vol. 105, pp. 420-433. COSTLOW,J. D. & C.G. BOOKHOUT,1956. Molting and shell growth in Balanus amphitrite nivens. Biol. Bull. (Woods Hole, Mass.), Vol. 113, pp. 224-232. DAVIES, P. S., 1967. Physiological ecology of Patella II. Effect of environmental acclimation on metabolic rate. J. Mar. Biol. Assoc. U.K., Vol. 47, pp. 61-74. DAVIES,C. W., U. H. FYHN & H.J. FYHN, 1973. The intermolt cycle of cirripeds: criteria for its stages and its duration in Balanus amphitrite. Biol. Bull. (Woods Hole, Mass.), Vol. 145, pp. 310-322. ELVIN, D.W. & J.J. GONOR, 1979.The thermal regime of an intertidal Mytilus cal@rnianus Conrad population on the central Oregon coast. J. Exp. Mar. Biol. Ecol., Vol. 39, pp. 265-279.
FORSTER,J. M. & P. A. GABBOTT,1971. The assimilation ofnutrients from compounded diets by the prawns Palaemon serratus and Pandalus platyceros. J. Mar. Biol. Assoc. U.K., Vol. 51, pp. 943-961. FUSARO,C., 1978. Growth rate ofthe sand crab, Emerita analoga, (Hippidae) in two different environments. Fishery Bull. NOAA, Vol. 76, pp. 369-375. FYYN, H. J., J. A. PETERSEN& K. JOHANSEN,1972. Eco-physiological studies of an intertidal crustacean, Pollicipes polymerus (Cirripedia, Lepadomorpha) I. Tolerance to body temperature change, desiccation and osmotic stress. J. Exp. Biol., Vol. 57, pp. 83-102. HILGARD,G. H., 1960. A study ofreproduction in the intertidal barnacle Mitellapolymerus in Monterey Bay, California. Biol. Bull. (Woods Hole, Mass.), Vol. 119, pp. 169-188. HINES, A. H., 1978. Reproduction in three species of intertidal barnacles from central California. Biol. Bull. (Woods Hole, Mass.), Vol. 154, pp. 262-281. HOWARD,G. K. & H. C. SCOTT, 1959. Predaceous feeding in two common gooseneck barnacles. Science, Vol. 129, pp. 717-718. HUBBELL,S.P., A. SIKORA & O.H. PARIS, 1965. Radiotracer, gravimetric and calorimetric studies of ingestion and assimilation rates of an isopod. Health Phys., Vol. 11, pp. 1485-1501. KUZNETSOVA,LA., 1973. Utilization of several kinds of feed by cirriped crustaceans. Hydrobiol. J., Vol. 9, pp. 33-40. LASENBY,D.C. & R.R. LANGFORD,1973. Feeding and assimilation of Mysis relicta. Limnol. Oceanogr., Vol. 18, pp. 282-285. LAWTON,J. H., 1970. Feeding and food energy assimilation in larvae of the damselfly Pyrrhosoma nymphula (Sulz) (Odonata: Zygoptera). J. Anim. Ecol., Vol. 39, pp. 669689. LEWIS, C.A., 1975. Some observations on factors affecting embryonic and larval growth of Pollicipes polymerus (Cirripedia : Lepadomorpha) in vitro. Mar. Biol., Vol. 32, pp. 127-139. LEWIS, C. A.,1981. Juvenile to adult shiR in feeding strategies in the pedunculate barnacle, Pollicipes polymerus (Sowerby) (Cirripedia, Lepadomorpha). Crustaceana (Leiden), Vol. 41, 14-20. LOSADA, F.J., 1975. Studies on growth and shell deposition in barnacles of the genus Balanus. Ph.D. dissertation, Duke University, 120 pp. PATEL, B. & D. J. CRISP, 1960. The influence of temperature on the breeding and the moulting activities of some warm water species of operculate barnacles. .I. Mar. Biol. Assoc. U.K., Vol. 39, pp. 667-680. RIISGARD, H.U. & A. RANDLOV,1981. Energy budgets, growth and filtration rates in Mytilus edulis at different algal concentrations. Mar. Biol., Vol. 61, pp. 227-234. SASTRY,A.N., 1975. Physiology and ecology of reproduction in marine invertebrates. In, Physiological ecology of estuarine organisms, edited by F. J. Vernberg, University of South Carolina Press, Charleston, pp. 279-300. SOKAL, R. R. & F. J. ROHLF, 1969. Biometry. W. H. Freeman and Co., San Francisco, 776 pp. STRAUGHAN,D., 1971. Breeding and larval settlement of certain intertidal invertebrates in the Santa Barbara Channel following pollution by oil. In, Biological and oceanographic survey of the Santa Barbara channel oil spill 196991970, Vol. I, edited by D. Straughan, Allan Hancock Foundation, University of Southern California, Los Angeles, pp. 223-244. STRICKLAND, J. D. H. & T. R. PARSONS,1968.Apracticalhandbookofseawater analysis. Bull. Fish. Res. Board Can., No. 164, 3 11 pp THOMPSON,R. J. & B. L. BAYNE, 1972. Active metabolism associated with feeding in the mussel Mytilus edults L. J. Exp. Mar. Biol. Ecol., Vol. 9, pp. 111-124. THOMPSON,R. J. & B. L. BAYNE,1974. Some relationships between growth, metabolism and food in the mussel Mytilus edulis. Mar. Biol., Vol. 27, pp. 3 17-326. UNIVERSITYOF CALIFORNIA,SCRIPPS INSTITUTIONOF OCEANOGRAPHY,197&1980. Surface water temperatures at shore stations. United States west coast.
‘02
H.M.
PAGE
WARREN, C.E. & G.E. DAVIS, 1967. Laboratory studies on the feeding, bioenergetics, and growth of fish. In, The biologicalbasis offreshwaterftFhproduction, edited by S. D. Gerking, Blackwell Scientific, Oxford, pp. 175-214. WIDWWS, J., 1978. Combined effects of body size, food concentration and season on the physiology of Mytilus edulis. J. Mar. Biol. Assoc. U.K., Vol. 58, pp. 109-124. Wr!, R. S. S. & C. D. LEVINGS, 1978. An energy budget for individual barnacles (Balmus gfandulo). Mar. Biol., Vol. 45, pp. 225-235.
189
Elsevier
EFFECT OF WATER TEMPERATURE AND FOOD ON ENERGY ALLOCATION IN THE STALKED BARNACLE, POLLICIPES
POLYMERUS
Sowerby
H.M. PAGE Marine Science Institute, University of California Santa Barbara, Santa Barbara, CA 93106. U.S.A. Abstract:
The effects of water temperature and. food level on absorption efficiency, rate of oxygen consumption, molting rate, reproductive condition, energy content, and total production have been studied in the stalked barnacle, Pollicipespolymerus Sowerby. Absorption efficiency measured gravimetrically was high (~94%) and unaffected by water temperature or food level. Absorption efficiency measured using an ash-ratio method was substantially less than that determined gravimetrically. The rate of oxygen consumption increased in the high food treatments and decreased in the starved treatment after 40 days. Molting rate, energy content, and total production were highest in the high food treatments. Reproduction was inhibited at warm water temperatures. The greater influence of food level than water temperature on production is probably related to the thermal regime experienced by these animals in the field.
INTRODUCTION
Water temperature and food availability have been shown to influence the growth and/or reproduction of a variety of marine intertidal invertebrate species (see for example, Barnes, 1963; Sastry, 1975; Bayne, 1976; Hines, 1978). Few studies, however, have considered the influence of these variables on growth and reproduction in the context of the total energy budget of the organism. Those experimental studies available on energy partitioning of intertidal species have been confined largely to mollusks. For example, at water temperatures > 20 ’ C, the energy available for growth of laboratory maintained mussels, Mytilus edulis, decreased as a result of increased metabolic rate and reduced filtering rate (Thompson & Bayne, 1974; Bayne, 1976). Similiar results were obtained on M. californianus from San Juan Island, Washington, at water temperatures > 22 “C (Bayne et al., 1976). Assimilation efficiency and the fraction of ingested energy available for growth and reproduction is dependent on food level in M. edulis (Thompson & Bayne, 1974; Widdows, 1978; Riisgard & Randlov, 1981) and in M. californianus (Bayne et al., 1976; Elvin & Gonor, 1979). By measuring changes in energy budget components in the laboratory, the present study investigated the influence of water temperature and food level on absorption efficiency and food energy partitioning in an intertidal crustacean, the stalked cirriped, Pollicipespolymerus Sowerby. This barnacle is frequently found associated with Mytilus cal~fimiunus and iU. edulis on exposed rocky shores and pier pilings along the Pacific coast of North America. In the Santa Barbara area, Pollicipespolymerus can experience 0022-0981/83/$03.00 0 1983 Elsevier Science Publishers B.V.
I90
H.M.PAGE
water temperatures ranging from 12 “C in late winter to > 20 ‘C in . late summer (University of California, 1970-1980; Neushul, unpubl. data). Highest brooding frequencies of P. polymerus are in the winter (Straughan, 197 1; Page, in prep.). Reproduction of P. polyments collected 60 km north of Santa Barbara was inhibited at water temperatures of 20 “C in the laboratory (Cimberg, 1981).
MATERIAL
AND
METHODS
P. polymerus were collected
on small pieces of rock from the mid-intertidal ( + 0.75-1.0 m M.L.L.W.) at Goleta Point, Santa Barbara, a soft shale headland along a protected outer coast bordering the Pacific Ocean. Ambient water temperature at the time of collection was 15.5 “C. Groups of three to five individuals were cleaned of adhering material and fastened with rubber bands to plastic stands. Within 24 h of collection four groups of 50 individuals each (16.0 + 1.Omm capitulum height, hereafter designated ch, k SD) were placed in separate recirculating whirlpools (Fig. 1).
A
Fig. I. Diagram
of experimental apparatus: arrows indicate direction of water flow; A, water inflow from reservoir: B, screen; C, water outflow to reservoir.
Whirlpools were used in each treatment to provide the proper environment for feeding. P. polyments (except for very small individuals, Lewis, 198 1) depend on water flow to carry food particles to their extended cirri. Sea water was pumped from a temperature controlled 100-l reservoir into the whirlpool through small nozzles producing rapid water flow. Water circulated around the whirlpool and through a bottom
ENERGY
ALLOCATION
IN POLLICIPES
POLYMERUS
191
screen which caught uneaten food, feces, and exuviae. The barnacles were orientated with the feeding apparatus facing the water flow. Each group of 50 barnacles was subjected to one of four treatments: cold water (13.2 + 0.9 ‘C, + SD) with high or low food ration (designated CH and CL, respectively) or warm water (19.8 f 0.5 ‘C) with high or low food ration (WH and WL, respectively) for 40 days (30 May to 8 July) in ambient light conditions. These water temperatures are typical of those experienced by P. polymenrs in the late winter and late summer in Santa Barbara. A control group of 15 barnacles was placed in cold water (13 “C) and starved. Each day either two (low ration) or 12 (high ration) brine shrimp adults (Artemiu salina (L.), San Francisco) per individual barnacle were added to the whirlpools. Artemiu adults were used for food for the following reasons : (1) they are easily counted, (2) they are easily recovered if uneaten, (3) they remain homogeneously suspended in the water column, and (4) they are similiar to the crustacean diet of Policipes polymerus in the field (Barnes, 1959; Howard & Scott, 1959; Lewis, 1981; Page, in prep.). The experimental animals were exposed to ambient air temperature for x 10 min each day while feces, exuviae, and uneaten Artemiu were removed. They were also exposed to air for up to 1 h every 4 days while water in the reservoirs was replaced and brought to the desired temperature. Forty specimens of P. polymerus, collected from the same location and of the same size (16.0 f 1.0 mm ch) as the experimental animals were sacrificed at the beginning of the experiment to estimate the initial energy content of barnacles used in each treatment. Five samples of 300 Artemiu were taken during the course of the experiment, rinsed several times in de-ionized water to remove adhering salt, and dried to a constant weight at 60 ‘C to estimate individual dry weight. The soma and any egg masses in the mantle cavity of barnacles were removed, rinsed in de-ionized water, dried to a constant weight at 60 “C and weighed. The remainder of each barnacle was frozen, then thawed to permit easy separation of the sheath from the stalk. Ovaries, if present, were removed from the stalk and both were weighed after drying at 60 ‘C. P. polymerus produce compact feces and these were also gently rinsed prior to being dried and weighed. The caloric content of the soma and stalk tissues, ovaries, food, exuviae, and feces was determined using a Parr 1411 microbomb calorimeter. Dried samples were ground to a fine powder with a mortar and pestle and pelletized prior to combustion. Subsamples were ashed at 450 “C for 24 h to determine ash-free dry weight (AFDW). ABSORPTION
EFFICIENCY
Efficiency of absorption of the Artemia salina by Pollicipespolymencs in each treatment was determined gravimetrically using both the dry weight and caloric content of the food and feces: A = [(C - F)/C] x 100, where A is the absorption efficiency, C the dry weight or calories of food ingested, and F the dry weight or calories of feces egested. Absorption efficiency was also determined using the ash-ratio method of Conover
H. M. PAGE
192
(1966). This method, frequently employed where the quantitative recovery of feces is impractical, assumes that only the organic fraction of the food is absorbed. The following formula was used for the calculation of absorption efficiency by this method: U = (F - E)/( 1 - E)F, where U is the absorption efficiency, E the organic fraction in the food, and F the organic fraction in the feces. OXYGEN
CONSUMPTION
Measurements of rate of oxygen consumption, obtained using four groups of two to three individuals (16 mm ch) at the beginning, mid-point, and end of the experiment provided estimates of the metabolic rate of individuals in each treatment. The same animals were followed over time. A temperature-controlled flow-through respirometer (180-ml capacity) was used. An air stone in the reservoir maintained the water at air saturation. A small magnetic stirring bar enclosed in the respirometer facilitated mixing. The small pieces of shale rock on which the barnacles were attached were rinsed in de-ionized water to remove adhering microorganisms prior to each measurement. Antibiotics may influence barnacle behavior (Cimberg, 1978) and were not used. Outflowing water (flow rate = 2 ml. min- ‘) was collected in a stoppered 50-ml Erlenmeyer flask. At the end of an experiment (6 h duration) the oxygen in samples of water flowing into the flask was determined by microburette titration (Winkler, from Strickland & Parsons, 1968). Oxygen consumed was the difference in oxygen concentrations between water flowing into and out of the respirometer multiplied by the flow rate. Respiration experiments were done in darkness. Controls without animals were run at both temperatures and did not exceed 10% of the oxygen consumed. This was taken into account when calculating respiratory rates.
RESULTS
ABSORPTION
EFFICIENCY
The number and dry weight of Artemia salina ingested by Poiiicipes polymer-us and the number of calories ingested and egested is given in Table I. The caloric content of the Artemia was 4747 k 46 cd. g dry wt.- ‘. Individuals in the high ration treatments ingested approximately five times as many calories as those in the low ration treatments. Absorption of ingested food measured using gravimetric techniques was unaffected by experimental water temperatures or ration and ranged from 93 to 95yj0 (Table I). The ash-ratio method greatly under-estimated absorption efficiency of Pollicipes polymerus producing values of from 26 to 41 “/b (Table I). The relatively small increase in the percentage of ash in the feces (16-19%) compared with that in the food (127;) indicates a high (= 90 ‘&) absorption of inorganic material (Table I). No data are available on the excretory losses of soluble materials. The excretory loss of other species feeding carnivorously is generally < 10% absorbed energy (Brett & Groves, 1979).
ENERGY
IN POLLICIPES
ALLOCATION
TABLE
Summary
193
POLYMERCJS
I
ofnumber, dry weight, and calories ingested as Artemiu salina and dry weight and calories egested as feces by Pollicipes polymerus in each treatment: for key to treatments see p. 191. Treatment
Initial no. barnacles Final no. barnacles Ration (no. Artemiu. ind- ’ . day- ‘) Aver. no. Artemia ingested. ind- ’ . day- ’ Total no. Artemiu ingested. ind-’ treatmentDry wt. Artemia ingested. ind- ’ (mg) Calories ingested. ind-’ Feces dry wt. ind- ’ (mg) Feces caloric content (Cal. gg ‘) Cal. egestedind- ’ Cal. absorbed. ind- ’ (ingested-egested) (A) Absorption efficiency (%) Dry weight Calories Ash-ratio Ash absorption (T,,)
BODY WEIGHT
AND CALORIC
’
CH
CL
WH
WL
50 50 12 8.9 356 126 598 7.7 4518 34.8 563
50 45 2 1.9 76 30 142 2.2 4493 9.9 132
50 46 12 9.2 368 129 611 6.7 4934 33.1 578
50 50 2 1.7 68 23 109 1.1 4476 5.1 104
93.9 94.2 37.5 90.9
92.6 93.0 40.7 88.4
94.7 94.5 26.3 93.1
95.1 95.4 33.9 93.0
CONTENT
Only barnacles at the higher temperature and with a high food ration increased in total body tissue weight (P < 0.05, Student’s t-test) (Table II). Barnacles starved for 40 days decreased in total body weight (P < 0.05, Student’s t-test). At the low temperature and with a high ration the caloric content (cal *g dry vv- ‘) of both soma and stalk tissues increased (Table II). MOLTING
FREQUENCY
Molting frequency in each treatment was calculated as the average number of molts produced per day for each consecutive lo-day period (Fig. 2). Two-way analysis of variance was done on square-root transformed data (Sokal & Rohlf, 1969) over each lo-day interval. No effect of water temperature or ration on molting frequency was evident between 1 and 10 or 11 and 20 days. A significant interaction (P < 0.001) between temperature and ration was found between 21 and 30 days, whereas ration alone influenced molting frequency between 31 and 40 days (P < 0.001). Unlike most crustaceans, the exuviae of barnacles contain little calcium carbonate. The ash fraction of P. polymenu exuviae was 7.1% (N = 39) and the caloric content 4356 f 106 cal .g-‘. Multiplying the average weight of an exuvium (5.6 x 10e3 g) by its caloric content gave an estimate of 24.4 calories per exuvium. One molt represented a loss of 1.5-2.0x of the energy content of the combined soma and stalk tissues.
body ueight
different
(P) (Acal
* Significantly
Production
Exuviae
’)
from initial sample
ind(P < 0.05).
_
264+ 67 1093 + 359 21 1378
4708 4633
Energy content (Cal. ind-‘) Soma Stalk Ovaries and brood Total
gm’ i
18 20 + 6 4+7
’
(cal
56& 14 236 + 51 292 + 71
Reproductive condition 0x brooding good wt (mg dry wt) Ovary wt (mg dry wt)
Exuviae Aver. no. ind-
Caloric content Soma Stalk
repr~lducti\e
Initial
(k SD).caloric cuntcnl.
Body weight (mg dry wt) Soma Stalk Total
A\cragc
+ 109
21 -_--_
270 + 53 1145 + 359 51 1466
25 1955 10 * 5*
1.19
4819 4934
56j, 11 232 + 63 288 f 84
-48
13
241 f 59 1044 f 386 31 1317
17 14+ 8 6+4
0.77
4717 4881
51+ 13* 214 + 52 265 t 73
CL
and change in energ! treatment see p. 191.
CH
condition,
T~BI F II
+ 156
28
248 + 54 1253 f 360* 5 1506
0* 0 1 +2*
1.75
4684 4692
53 * 12 267 k 72* 320 + 60*
WH
(production)
Treatment
content
WL
III each treatment:
-48
21
210+ 73* 1094 f 430 5 1309
0* 0 1 + t*
1.20
4651 4655
45 + 16* 235 k 48 280 + 62
of barnacle>
_
-272
7
225 k 37* 870 + 198* 5 1099
0* 0 1+ _- 7*
0.47
4694 4620
48 f 8* 188+40* 236 k 35*
Starved
for key to
z
2
z
ENERGY ALLOCATION IN POLLZCZPZS Z’OLYMERLIS
l-10
11-20 TIME
21-30
195
31-40
(days]
Fig. 2. Molting frequency of barnacles in the fed treatments: average number of molts per day asker square-root transformation.
REPRODUCTION
There was a decline in the percentage of barnacles carrying egg masses in the warm water treatments after 40 days (P < 0.05, chi-square test) and the average weight of ovary also decreased (P -C0.05, Student’s c-test) (Table II). Neither high nor low food ration had a significant effect on reproduction at either water temperature. The percentage carrying egg masses (P -C0.05, chi-square test) and average weight of ovary (P < 0.05, Student’s t-test) did, however, decline during starvation. The caloric content of well-developed ovaries was 5128 f 15 cal *g dry wt-‘. The time of development ofP. polymerus embryos (25-30 days, Hilgard, 1960; Lewis, 1975) and the stage of development (early or intermediate) suggest that egg masses in the mantle cavity of barnacles in the cold water treatments were produced sometime during the 40-day period. ENERGY CONTENT
The energy content of the soma, stalk, ovaries, and egg masses of barnacles in the intial sample and in each experimental treatment was determined by multiplying tissue dry weight by the corresponding caloric content. These values, summed with the energy lost in the production of exuviae, were compared with the initial sample to estimate the “actual” change (sensu Riisgard & Randlov, 198 1) in individual energy content during the experiment (production, P, Table II). Ration, rather than water temperature, had the greatest influence on change in total energy content. Total energy content increased in the high ration treatments and decreased in the low ration and starved treatments. The increase in energy content of barnacles in WH was due primarily to an increase in weight. By contrast, an increase in caloric content and the production of ovarian tissue contributed to the increase in
IYh
H.M.
PAGE
energy content of barnacies in CH. The decrease in energy content of starved barnacles was due primarily to a 20% decrease in weight. OXYGEN
CONSUMPTION
The results of respiratory measurements on barnacles from each treatment at the beginning, mid-point, and end of the experiment are given in Table III. Because it was not possible to weigh accurately individual barnacles attached to small rocks and because of the possibility of body weight or compositional changes during the experiment, the results are expressed per ~di~du~ rather than per g weight. TABlk
111
Rate of oxygen consumption of barnacles in experimental treatments (see p. 191): the same ammals measured over time; average of four determinations + SD. Rate of oxygen consumption rreatment
(ml.
h- ’ ind ’ i
Day 0
Day 20
Day 40
CH CL.
0.074 + 0.009 0.073 + 0.009
0.079 i 0.024 0.073 * 0.019
0.127 * 0.027*
WH WI.
0.106 + 0.009 0.090 * 0.014
0.118 k 0.02P 0.08Y -t_0.027
0.134 + 0.007* 0.090 + 0.030
0.077 fr 0.00’)
0.074 -i: 0.007
0.059 + o.u07*
Starved * Signi~cantly
(13 “C) different
from Day 0 (P < 0.05, Student’s
were
fJ.064
2 0.1820
t-test).
At Day 0, the respiratory rate of barnacles in the warm water treatments was signif?cantly higher than those in cold water (Q10 = 1.57) (P < 0.05, Student’s t-test). With time, however, the respiratory rate of barnacles fed the high ration in both temperature treatments increased and was higher than those on low food after 40 days (P < 0.05, Student’s t-test). The respiratory rate of starved P. polyrnerus declined after 40 days (P < 0.05, Student’s t-test). To determine whether the increase in individual respiratory rate in the CH and WH treatments was due to an increase in body weight, an estimate of oxygen consumption per dry weight (ml . g dry wt- ’ . h.- ‘) at Day 40 was made (Table IV). Since barnacles were not weighed until the end of the experiment, the estimate of weight-specific respiratory rate for each treatment at Day 0 was made using the average dry weight of the initial sample. The weight-spec~c respiratory rate of well-fed barnacles increased independently of an increase in body weight. Two estimates of the fraction of absorbed energy expended in respiration are derived from the general energy budget equation A = R + P + E, where A is the absorbed energy (calories), R the energy used in resp~ation, and P the production measured as changes in energy content, including molt and ovary production (Table IV). The excretion of soluble materials (E) was not taken into account in these calculations.
ENERGY
ALLOCATION
IN POLLICIPES
POLYMERUS
197
The first estimate was obtained by subtracting production (P) (Table II) from absorbed calories (A) (Table I). This estimate assumed a balanced energy budget (R = A - P). In the second estimate, the amount of oxygen consumed by barnacles in each treatment, estimated separately for the first 20 days and the second 20 days from Table III, was multiplied by 4.8 cal . ml 0; ’ (Brody, 1945) to yield the calories expended in respiration (Table IV). This value was divided by absorbed calories (Table I) to calculate the respiratory fraction. TABLE IV Estimates
ofweight-specific respiratory rate, respiration fraction, and scope for growth for barnacles treatment (see p. 191): + , estimated using average body dry weight of initial sample.
CH
CL
WH
WL
in each
Starved
Oxygen consumption rate (ml O,.g dry wt-‘.h-‘) Day 0’ Day 40
0.24 0.44
0.23 0.24
0.34 0.42
0.32 0.32
0.24 0.25
Respiration fraction Estimate from production (1 -P/A)
0.81
1.36
0.73
1.46
_
Estimate from 0, consumption (R/A )
0.73
2.42
0.88
3.96
-
Estimated calories expended in respiration from 0, consumption measurements
411
319
509
412
314
Scope for growth
(A - R)
+ 152
-187
+69
-308
-314
Estimates of the respiratory fraction made from oxygen consumption data were appreciably higher than those determined from measuring production in the low ration treatments (Table IV). No consistent pattern was evident with water temperature. Estimated caloric losses in respiration (Table IV) alone were from 1.3 (respiration estimate) to 2.7 (production estimate) times greater in barnacles in the high ration than low ration treatments. SCOPE
FOR
GROWTH
The number of calories used in respiration (R) was subtracted from absorbed calories (A) to yield the “scope for growth”, (Warren & Davis, 1967), the “estimated” energy available (sensu Riisgard & Randlov, 1981) to barnacles in each treatment for growth and reproduction (Table IV). The high ration treatments, at both water temperatures had a positive scope for growth, indicating that energy was available for growth and reproduction. A negative scope was found for barnacles in the low ration and starved treatments, indicating that these barnacles were metabolizing their body tissues for
H.M. PAGE
19x
m~nt~n~ce. The scope for growth and the production estimates were in agreement on whether energy was gained or lost by barnacles during the experiment. The actual values differed, however, between these two estimates, particularly for the low ration treatments. MAINTENANCE
RATION
The maintenance ration of submerged P. polymerus (16 mm ch) was estimated using data on the scope for growth (Table IV) and the energy content decrease (Table II) of starved specimens. The oxygen consumed by starved barnacles converts, using 4.8 Cal. ml 0; ’ , to a maintenance energy expenditure of z 7.9 Cal. ind ’ . day ’ . The maintenance ration estimated from a decrease in body weight (P) is slightly lower; 6.8 Cal. ind- ’ . day- ’ (272 cal in 40 days). DISCUSSION
The absorption efficiency of P. po&merus feeding on Artemia salina was not affected by a five-fold difference in ration or a seven degree difference in water temperature. These results are consistent with the hypothesis that the absorption efkkiency of invertebrates feeding carnivorously is relatively inflexible, being influenced primarily by type of food (Lawton, 1970). By contrast, the absorption efficiency of herbivores and detritivores appears more flexible. For example, the absorption efficiency of ~yti~us edulis feeding on algae was inversely related to food level and perhaps water temperature (Thompson & Bayne, 1974; Bayne, 1976; Widdows, 1978). Absorption efficiency was inversely related to ingestion rate in the isopod, Armadillidium vulgare, (Hubbell et al., 1965) and the snails, Ancylus jluviatilis and Planorbis contortus, (Glow. 1975). Absorption efficiency for two other barnacle species fed Artemia salina nauplii exceeded 90ya : Balanus improvisus (94%) (Kuznetsova, 1973) and Balanus glanduIa (99%) (Wu & Levings, 1978). Absorption efficiency of Pollicipespolymerus was under-estimated when determined by the ash-ratio method. Similiar results have also been noted for chaeto~aths (Cosper & Reeve, 1975), shrimp (Forster & Gabbott, 1971) and mysids (Lasenby & Langford, 1973). The under-estimate in the present study was due to the high assimilation of ash by P. po!vmerus. This indicates that food is a potentially important source of minerals for shell production in this species. Few data are available on the effect of food and water temperature on the molting frequency of P. polymerus or other temperate-water barnacles. The molting frequency of P. polymerus (16 mm ch) does not appear great. An estimate of intermolt interval can be obtained using the “instantaneous” method (Fusaro, 1978) over the first ten days of the experiment: f, = t/p,, where f,, is the intermolt interval in days, t the total number of days held (10 days), and pt the proportion of individuals which molted in t (10) days. The estimate of a 40-day intermolt exceeds values (generally < 7 days)
ENERGY ALLOCATIQNIN
~~LLZCZ~ESFOLY~E~WS
199
reported for other temperate-water barnacles (Costlow & Bookhout, 1953,1956; Davis et al., 1973 ; Losada, 1975). The weight loss and energy loss on molting appear small ( w 2.0% ), consistent with the estimation on ~~i~~~ g~~~~~~ of 2.3 % (Wu & Levings, 1978). The high molting rate of Pollicipespolymerus in WL between 2 1 and 30 days followed by the drop between 31 and 40 days, in comparison with the continued increase in WH suggests that warm water may accelerate molting and deplete energy reserves after 30 days. A similiar pattern, on a shorter time scale, was found for the boreo-arctic species, Balanus buhnoides (Pate1 & Crisp, 1960). Food level appeared most important and acted in combination with water temperature. The molting rate of fed B. baianoides increased linearly with water temperature from 3 to 20 “C. The increased molting rate at higher temperatures apparently, however, utilized food reserves more rapidly, resulting in a reduced rate when food was withheld (Pate1 & Crisp, 1960). The increase in respiratory rate of Pollicipes polymer-us on high ration was probably related to changes in the nutritional state of these barnacles. Seasonal changes in the oxygen cons~ption rate of Balanus bul~~ides was attributed, in part, to seasonal changes in the level of food supply (Barnes et al., 1963). Thompson & Bayne (1972) found an increased oxygen requirement resulting from the presence of food in the guts of Mytilus edulis. Davies (1967) correlated higher respiratory rates of limpets (Patella ~~g~t~) with high av~labi~ity of food and suggested higher respiratory rates may be associated with active somatic and reproductive growth. The influence of water temperature on the measured respiratory rate of freshly collected Pollicipes polymerus although significant, was small (Qlo = 1.57). No consistent influence of water temperature was found on the “actual” or “‘estimated” energy available for growth and reproduction. Although good agreement between the two estimates was obtained for the high ration and starved barnacles, the measured respiratory rate of individuals in the low ration treatments was higher than predicted from changes in energy content. These results are similiar to those obtained by Riisgard & Randlov (198 1) on Myths edulis and suggest that the low ration animals became more active during respiration experiments. The results of the respiratory studies on Pollicipespolymerus conducted by Barnes & Barnes (1959) cannot be compared directly with those of this study since they measured rates of the soma alone and their results are expressed per g *wet wt- ’ at 10 “C. A respiratory rate of 0.05 ml O2 * g- ’ +h- * for an animal of 200 mg wet weight from Barnes & Barnes (1959) converts to 0.25 ml 0, *g dry wt- ’ . h-’ (assuming the soma is 80% water; Page, unpubl. data) which agrees well with the values for the starved and low food animals measured at 13 “C at the end of the present experiment. The greater influence of food rather than environmental water temperature in influencing estimated and actual production for P. polymerus is not surprising given the intertidal existence of this organism. Fyhn et al. (1972) found the body tissue temperature of P. polymerus was equal to that of ambient sea water when submerged, but could increase during air exposure. Bvin & Gonor (1979) showed that the mussel, ~~fj~~~
X(1
H.M. PAGE
~~~z~~~j~~~~, also experiences short-term thermal shocks from exposure to air, coastal upwelling, and other factors. This mollusk, as well as M. edzdis,is capable of maintaining a relatively constant rate of oxygen consumption over a wide range of environmental water temperatures. Above certain critical water temperatures, however, the scope for growth declined as a result of a sharp increase in the energy devoted to metabolism. Critical water temperatures, which elicit a sharp increase in respiratory rate, appear to exceed 20 ‘C for Pollicipespolymerus from Santa Barbara. Water temperature strongly influenced the amount of absorbed energy partitioned to somatic and reproductive tissues in P. poIymerus. The implications of these results for field conditions are that, given a constant amount of food, there can be an energy “trade-off’ between reproduction and growth (or storage) regulated by water temperature.
ACKNOWLEDGEMENTS
I thank Drs. A. Wenner, A. Kuris, D. Morse, and J. Childress as well as S. Willason, T. Mickel, and P. Hiller-Adams for helpful comments on the manuscript. I also thank F. Dewitt and P. Siegel for technical assistance and J. Popp for drawing the apparatus. Funding was provided by the Marine Science Institute and a University of California Patent Fund grant. REFERENCES BARNES.H., 1959. Stomach contents and microfeeding of some common cirripedes. Can. J. ZooI., Vol. 37. pp. 231-236. BARNES.H., 1963. Light, temperature, and the breeding of Balanus balanoides. 1. Mur. Biol. Assuc. U.K., Vol. 43, pp. 7 1l-727. BARNES,H. & M. BARNES. 1959. Studies on the metabolism of cirripedes. The relation between body weight, oxygen uptake, and species habitat. Verofl Inst. ~eeres~rsch., Bremerhaven, Vol. 6, pp. 5 15-523. BARNES,H., M. BARNES& D.M. FINLAYSON,1963. The seasonai changes in body weight, biochemical composition, and oxygen uptake of two common boreo-artic cirripedes, Bahnus halanoides (L.) and Bultmus balanus (L.). J. Mar. Biol. ,4ssoc. U.K., Vol. 43, pp. 185-21 I.
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