Bulletin of the Japanese Society of Scientific Fisheries 49(1), 33-40 (1983)

Bioenergetics of the Benthic Herbivorous Populations in a Rocky Intertidal Habitat

Mitsuhiro NAGATA* (Received May 31, 1982)

Energy transformations through the population of rocky intertidal herbivores, Strongyl ocentrotus intermedius, Chlorostoma argyrostoma turbinatum and rusticus, were ana lyzed from Oct. 1978 to Oct. 1979, using estimates of average weight and numbers of individuals in each size-group and observations on respiratory rates. The energy entering the population, which is the sum of the energy assimilated as food and the rate of immigrants, was 118.4 Kcal m-2 yr-1 for the Strongylocentrotus population, 12.6 Kcal m-2 yr-1 for the Chlorostoma popula tion, and 6.6 Kcal m-2 yr-1 for the Omphalius population. The amount of energy lost from the population, expressed as respiration, gametes ejected, predation, mortality and emigration, was estimated at 119.6, 13.4 and 6.5 Kcal m-2 yr-1 for the Strongylocentrotus, Chlorostoma and Omphalius populations, respectively.

Since the rocky intertidal regions are strictly Hokkaido. The low-tide-platform, which meas exposed to changes in many environmental ured about 58.6•~104m2 in area, is about 3000 m factors, the rocky intertidal fauna is characterized along the shore-line and about 200m off-shore. largely by fluctuation in aspects of community The tidal excursion at this site is about 0.6 m in structure, including space utilization patterns, vertical distance, and 80% of the platform is composition, trophic structure, and body size exposed at low water. Mean sea temperature structure. For example, studiesl-2) in rocky in ranges from a maximum of 26•Ž (August) to a tertidal fauna suggest that patterns of space utili minimum of 4•Ž (March). zation and size structure of predominant Invertebrate organisms in this community reflect the operation of important organizing include gastropods, bivalves, barnacles, arthro agents within the community. Therefore, we feel pods and echinoids as major components, and that close attention needs to be paid to the varia are similar to those in other rocky intertidal tions in certain aspects of community structure of habitats in southern Hokkaido. Of these species, rocky intertidal fauna, and that further information Strongylocentrotus intermedius, Chlorostoma concerning the population dynamics and produc argyrostoma turbinatum and Omphalius rusticus tivity of the predominant members is necessary are more abundant in biomass and density, over for a better understanding of the rocky intertidal the year, than others. benthic fauna. However, few reports3-7) have been published concerning the bioenergetic studies Methods on the grazer and deposit-feeder populations as major components of the community. In the The present study is based on the bimonthly present study, the specific objective were to clarify samples of the above three species taken from the population structure and to assess the annual the low-tide-platform from October, 1978 to population production of the predominant mem October, 1979. The abundance of these species bers of each species within a rocky intertidal was measured by counting the number of speci community located to the low-tide-platform in mens found in a known area of the seafloor at a Moheji. right angle with the shore-line; a quadrat of 1m2

(1•~1m) area was put on the sea-floor of 20m intervals along the tapeline. Thus, the popula Study Area tions were examined all along the regular eighteen The study site (Fig. 1) was located on the west sections running out from shore-marks a-r, as side of Hakodate Bay, along the coast of southern shown in Fig. 1.

* Faculty of Fisheries, Hokkaido University, 1-1 Minato-3, Hakodate 041,Japan(永 田 光 博:北 海 道 大 学

水 産 学 部). 34 NAGATA

Fig. 1. Diagramatic representation of topograph (A), sampling station (B), and mean surface sea temperature (C). In the top figure, each Arabic number shows the depth in meter.

The test diameters of Strongylocentrotus ob of body size distribution. The measurementsof tained by this procedure were measured, and this body size were divided into groups each represent was followed by the removal of gonad tissue. ing a range of 2mm in test diameter for Stron After measuring the shell diameter of Chlorostoma gylocentrotus and 1mm in shell diameter for and Omphalius, shell and body tissue, including Chlorostoma and Omphalius. Then the frequency gonads were removed separately. These tissues of each , group was represented by percentage. were placed in a drying oven at 60•Ž for three The bimodal frequency distribution obtained was days, until constant weight was achieved. After graphically analyzed by making use of a pro drying, the weight was measured. The dry sub bability graph paper method derived from stances were minced, and they were stored in a HARDING.9)The size-frequency distribution of desiccator to analyze caloric content by means of each group is represented in Fig. 2, together with

YM-Nenken digital type adiabatic bomb calo several fitted normal curves which were calculated rimeter. by this procedure . By this process, it is possible The rates of oxygen consumption of the to determine the growth rate of the mean body were determined bimonthly over a wide range of size of each size-group and to estimate the size sizes under the "closed system". An group structure in percentage occupancy. The oxycalorific equivalent') of 4.83 cal m1-1 O2 was results are illustrated in Table 1, and Fig. 3, re used to convert oxygen consumption to energy spectively. In the Strongylocentrotus population, units. II-size-group represents the distinguished per centage occupancy (75-90%) over the year.

Results Therefore, even if the quantitative fluctuation of the population was replaced by that of II-size Population Structure group, it would be unlikely for the estimates to The size structure was estimated on the basis be biased. It is possible to calculated the popula- Bioenergetics of the Benthic Herbivorous Populations 35

Fig. 2. Histogram showing the size frequency and several fitted normal curves calculated by the probability graph paper method. A: Strongylocentrous population, B: Chlorostoma popula tion, C: Omphalius population.

Table 1. Seasonal changes in the average test diameter (mm) of Strongylocentrotus intermedius and in the average thell diameter (mm) of Chlorostoma a. turbinatum and Omphalius rusticus 36 NAGATA

weight of individual body components belonging

to various size-groups as a function of mean shell or test diameter. Here the weight of each

size-group is estimated as the product of the number of individuals and the mean weight. The

sum of the weight of the separate size-groups

gives the biomass (Table 4).

Respiratory Rate

In general, it is well known that the logarithm

of oxygen consumption (R) is linearly related to

the logarithm of an individual dry weight (W). The exponential equation is R=aWo, where a is a

constant, and b is a regression coefficient. Fig. 4

shows the oxygen consumption per unit time per

animal plotted against dry body weight on loga

rithmic scale. Although the regression coefficient differs with season (Ft0.05)=2.53>F0=1.52 for

Strongylocentrotus, F(0.05)=3.58>F0=3.32 for

Chlorostoma, F(0.05)=2.50>Fo=2.37 for Ompha Fig. 3. Size-group composition of Strongylocen lius), there was clearly a seasonal change in the trotus population (a), Chlorostoma population respiratory rates over the whole range of animal (b), and Omphalius population (c). ?? : 0 size-group, ?? : I size-group, ?? : II size sizes. When the constant a in the oxygen con sumptiondry body weight regression equation group, ?? : III size-group, ?? : IV size-group, ?? : V size-group. was plotted against temperatures of 6.0•Ž to 22.2•Ž, came close to forming a straight line. tion size for the entire area of the platform on Consequently, it is possible to express oxygen the basis of the average density and size-group consumption (R) as a function of temperature (t) structure in percentage occupancy. This estimate and body weight (W), as shown below: is shown in Table 2. Strongylocentrotus log R=log (0.0070t+0.052) It is generally agreed that the logarithm of an +0.9351 log W individual dry body weight or of dry weight of Chlorostoma log R=log (0.1021t-0.5896) gonad tissue is linearly related to the logarithm +0.7887 log W of body size. These equations lead to dry weight Omphalius log R=log (0.0913t-0.4612) for an individual body or gonad from mean body +0.7951 log W size (shell or test diameter) in each size-group These equations are used to estimate the respira belonging to the total population. The regression tory metabolism of each of the above three animal statistics are illustrated in Table 3. The above populations as a function of sea temperature, dry equations were used to estimate the mean dry weight, and population size. Then the energy

Table 2. Population sizes in number per square meter. Each Roman number indicates size group Bioenergetics of the Benthic Herbivorous Populations 37

Table 3. Dry weight of body components (body and gonad: g, shell and flesh: mg) regression statistics at several body size (test and shell diameter: mm) Strongylacentrotus intermedius

Table 4. Changes in the biomass (g/m2) of the three benthic populations with the progressive months 38 NAGATA

Fig. 4. Logarithmic plot of respiratory rate against body weight. •¤: Oct. (15.5•Ž), •£: Dec.

(10.2•Ž), •¢: Mar. (6.0•Ž), • : Apr. (12.0•Ž), •œ: June (18.0•Ž), •¡: Aug. (22.2•Ž), •›: Oct. (16.0•Ž). (A): Strongylocentrotus population, (B): Chlorostoma population, (C): Omphalius population.

lost by metabolic activity is easily estimated from tion: the indirect method of respiratory rate into heat Final biomass-Initial biomass

output by the application of an oxycalorific coef =(Immigration+Assimilation)-Gametes

ficient. PAiN4) reported that the rate of aerial ejected-(Mortality+Predation+ respiration in an individual funebralis was Emigration+Yield) approximately half the rate of aquatic respiration, The magnitude of population increment at and he calculated annual respiration by assuming tributed to individual growth is taken to be the 75•“ of the gas exchange takes place in sea water. difference between the initial and final body In the present study, the rate of oxygen consump weight multiplied by the arithmetical mean of the tion and computation of annual respiration for initial and final population density. If it is posi the two gastropod populations were derived from tive, the difference between the initial and final the above data given by PAIN.4) There are 67.6 population density multiplied by the arithmetical Kcal m-2 yr-1 in the Strongylocentrotus popula mean of the initial and final body weight corre tion, 6.8 Kcal m-2 yr-1 in the Chlorostoma popula sponds to the magnitude of immigrants. If it is tion, and 3.9 Kcal m-2 yr-1 in the Omphalius negative, on the other hand, the above computa

population. tion is taken to be the population loss attributed to mortality, emigration, predation and yield. Annual Energy Budget The annual production of the population is the The quantitative equation representing me sum of the growth increment for individuals, the tabolism of an animal population is represented recruited members and immigrants. In the pre as follows10): sent paper, yield and loss of gametes, ejected from Initial biomass+Consumption+Immigration the gonad growth, are excluded with the exception =Egesta+Excreta+Respiration+ of those for the Strongylocentrotus population. Predation+Shedding+Mortality+Yield+ From the bimonthly values for the caloric con Emigration+Final biomass tent of each body component (Table 5), the popula where, tion production as energy unit may now be esti Consumption-(Egesta+Excreta) mated. A diagram of annual energy flow facili =Assimilation=Growth+Respiration tates the description of the flux and allocation of The growth is divided into two parts; that is , energy through a population. Figure 5 shows body growth and gonad growth. The increment schematically the rate of energy flow through the of individual numbers is attributed to immigra benthic populations of the Moheji rocky low tion and recruitment. The item of shedding in tide-platform. The energy entering the popula sea urchins and gastropods nearly corresponds to tion is the sum of the energy assimilated as food the gametes ejected. Consequently, the met and the rate of immigrants. These values for the abolic relation is replaced by the following equa Strongylocentrotus population were 108.4 Kcal Bioenergetics of the Benthic Herbivorous Populations 39

Table 5. Caloric value (Kcal/g) of the body (Upper column) and gonad (lower column) in St. intermedius and of the flesh in Ch. a. turbinatum and O. rusticus

Fig. 5. Scheme showing the annual energy budget of three benthic populations. The arrow indicates the direction of energy conversion. The shadow area shows a difference between initial and final biomass. Rates are Kcal m-2 yr-1. Initial biomass is Kcal m-2.

m-2 yr-1 and 10.0 Kcal m-2 yr-1, and 118.4 Kcal were based on the following assumptions: the m-2 yr-1 was the total input rate of energy. On growth of the two populations of gastropod species the other hand, the total amount of energy on included an increment of the body weight owing the debit side during a whole year was 119.5 to carrying the eggs, and the caloric content of Kcal m-2 yr-1, including metabolic loss (67.6 shell in the gastropod was regarded as zero Kcal m-2 yr-1), gametes ejected (20.2 Kcal m-2 calorie. The first assumption would be unlikely yr-1) and the sum of emigration, mortality, to be significantly biased, because the gonad predation and yield (31.7 Kcal m-2 yr-1). For weight accounted for only 2% of the total body this reason, the value of -1.1 Kcal m-2 yr-1 is weight. Caloric content of shell in mollusca4.11) equal to the energy stored in the Strongylocen has been reported to be 20-60 cal g-1. This trotus population during a whole year. For the value is notably lower than the caloric content of Chlorostoma and Omphalius populations, the co flesh (3000-5000 cal g-1). HUMPHREYS12)found ordinate values of -0.8 and 0.1 Kcal m-2 yr-1, that the logarithm of metabolic loss (R Kcal respectively, are estimated in the same manner. m-2 yr-1) and the logarithm of production (P Kcal m-2 yr-1) of non-insect invertebrates, in which category echinoid and gastropod lie, fell Discussion close to a regression line, as given by the follow ing equation: It should be noted that the estimates of the productivity on the three benthic populations log P=-0.366+0.942 log R 40 NAGATA

The predictive values of production for the sumed energy. As the energy input of the her Chlorostoma population (2.6 Kcal m-2 yr-1) and bivorous benthic community would be wholly for the Omphalius population (1.5 Kcal m-2 yr-1) dependent on the productivity of the algal com were found to be similar to their actual values munity, clarifying the population dynamics and (3.2 Kcal m-2 yr-1 and 1.5 Kcal m-2 yr-1). From bioeconomics of various algal populations and the above prediction, even though the computa various herbivorous benthic populations would tion of the calorie of molluscan shell is neglected, lead to an understanding of the rocky shore com it is obvious that the second assumption would munity structure and function. not cause a biased estimate of the production. From the energy budget obtained in the present study, various energetic efficiencies are calculated Acknwledgements which give the proportions of energy utilized for The author wishes to express his hearty thanks each metabolic process. Assimilation efficiency to Prof. A. Fun and to Associate Prof. S. NAKAO and ecological efficiency are the most relevant of Hokkaido University for their invaluable advice because they represent the proportion of the during the course of the present study and for their energy allocated by the organism population kindness in reading the manuscript. He is also which is actually available for growth and respira tion. Of these efficiencies, assimilation efficiency grateful to Messers. T. OCHIAI, M. YAMAZAKI,and K. FUJINAGAfor their continued assistance during is highly variable depending on the species, the the survey period, and to Miss T. HIRAI for pre age of the organism, the type of food and its density, internal physiological factors, the envi paring and typewriting the manuscript. ronmental conditions, and the way in which it is measured.13) Although assimilation efficiency References is important to the individual organisms, particu larly in nutritional considerations where opti 1) R. T. PAIN: Am. Nat., 103, 91-93 (1966). 2) B. A. MENGE: Ecol. Monogr., 46, 355-393 mization of feeding and growth are desired, com (1976). parison of data for different specific populations 3) R. T. PAIN: Ecology, 50, 950-961 (1969). would be of little value. The most important 4) R. T. PAIN: Limnol. Oceanogr., 16, 86-98 (1971). factor in comparing the magnitude of the energy 5) A. Fun and K. KAWAMURA:Bull. Japan. Soc. flow into and out of a trophic level is the ecological Sci. Fish., 36, 763-775 (1970). efficiency. SLOBODKINl4) defined ecological ef 6) R. N. HUGHES: J. exp. mar. Biol. Ecol., 6,167- ficiency as the relation of the steady state yield to 178 (1971). energy consumed. As far as the feeding habits 7) R. N. HUGHES: Mar. Biol., 11, 12-22 (1971). of echinoid and gastropod are concerned, they 8) V. S. IVLEV: Biochem. Z., 275, 49-55 (1934). are epistrate herbivores, and the assimilation ef 9) J. P. HARDING: J. mar. biol. Assoc. UK., 28, ficiencies of 0.45-0.83 have been reported for 141-153 (1949). several herbivorous echinoids15,16) and gastro 10) A. MACFADYEN: Grazing in Terrestrial and Marine Environments, Blackwell Sci. Publ., pods .17) Assuming for the moment that the as- Oxford, 1962, pp. 9-24. similation efficiency is 0.60, the value of 0.11 for 11) R. N. HUGHES: J. Anim. Ecol., 39, 357-381 the Strongylocentrotus population, 0.19 for the (1970). Chlorostoma population, and 0.17 for the Ompha 12) W. F. HUMPHREYS: J. Anim. Ecol., 48, 427-453 lius population correspond to the ecological (1979). efficiency. ODUM and SMALLEY16) found the 13) K. PETRUSEWICZand A. MACFADYNE: Produc average ecological efficiency to be 0.06 for the tivity of Terrestrial Animals-Principles and herbivorous invertebrates in a salt mash ecosystem, Methods, IBP Handbook No. 13, BlackwelI Sci. and PAIN4) gives 0.16 for the Tegula funebralis Publ., Oxford, 1970, pp. 112-115. population. SLOBODKIN14) suggested that the 14) L. B. SLOBODKIN: Am. Nat., 94,213-236 (1960). ecological efficiency of an aquatic system should 15) A. FUJI: Japan. J. Ecol., 12,181-186 (1962). 16) P. J. GREENWOOD:Estual. Coast. Mar. Sci., 10, have a value between 0.05 and 0.20. This re 347-367 (1980). latively high ecological efficiency suggests that the 17) T. H. CAREFOOT:J. mar. biol. Assoc. UK., 47, benthic herbivores inhabiting rocky low-tide 565-590 (1967). platforms may be adapted to the physical extremes 18) E. P. ODUM and A. E. SMALLEY: Proc . Nat. and are fairly efficient in the utilization of con Acad. Sci., 45, 617-622 (1959).