Journal of Coastal Deveolpment ISSN : 1410-5217 Volume 11, Number 2, February 2008 : 89-96

ECOLOGICAL ENERGETICS OF TROPICAL testudinaria (Linnaeus, 1758) LIVING ON THE ROCKY SHORE OF OHOIWAIT, SOUTHEAST MOLUCCAS, INDONESIA

Abraham Seumel Khouw

Faculty of Fisheries and Marine Sciences, Pattimura University, Ambon Indonesia

Received : November, 2, 2007 ; Accepted :January,4, 2008

ABSTRACT

Study on ecological energetics of tropical limpet C. testudinaria has been carried out at approximately one year from October 2001 to September 2002. Population energy budgets estimated on the assumption of steady state conditions for C. testudinaria (Linnaeus, 1758) on the rocky shore of Ohoiwait, are presented. Large difference in population structure, and hence energetics, occurred at different localities along the rocky shore. Relatively high proportions (98 %) of the assimilated energy was lost via metabolism. Assimilation efficiency is 39 %, net growth efficiency is 1.8 %, and ecological efficiency 0.3 %. Production (P), energy flow (A) and total energy consumption (C) were expressed as functions of size, in order to facilitate gross estimations of the energy component for which data on size frequency and density are available.

Key words: ecological energetics, , energy components

Correspondence: Phone : +6281343044295, e-mail: [email protected]

INTRODUCTION

Cellana testudinaria is intertidal, grazing Little has been published on the gastropod abundant on medium to very ecology of C. testudinaria. Khouw (2002) exposed rocky shores of Ohoiwait. The discussed their growth pattern and shell shows marked zonation, with only a shape variation in relation to zonal little overlap between zones. C. testudinaria distribution. Distribution, abundance, and occurs at several spatial and temporal scales biomass were investigated by Khouw from the extreme low water spring tide (2006a) and presented evidence for the (ELWST) to the extreme high water spring effects of drying. For several years, the tide (EHWST) and above EHWST in more recruitment pattern and productivity of this exposed situation, where it is almost species have been studied at the rocky shore continually splashed by wave action but of Ohoiwait (Khouw, 2005; 2006b). Work seldom actually submerged. Tide of has also been done on the growth Ohoiwait’s intertidal is mixed tide determination of this species (Khouw, prevailing diurnal type, with the average 2007). “spring” of about 1.5 m and “neap” of about The purpose of the study presented 1 m. here was to augment the data on growth

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Journal of Coastal Deveolpment ISSN : 1410-5217 Volume 11, Number 2, February 2008 : 89-96

rates, spawning and respiration with further Southeast Mollucas, Indonesia (Fig. 1) from observations on population structure, October to November 2007. The intertidal defaecation rates and the caloric contents of region investigated is about 0.25 km2 (1 km tissues and faeces, in order to compile long and 0.25 km wide). Thus, it is small population energy budgets for Cellana enough that atmospheric conditions may be testudinaria on the rocky shore of Ohoiwait. assumed, for most purposes, to be uniform over the whole area. The shore consisted of singles, pebbles, medium and big boulders of about 90% of covering substrate. The ATERIALS AND ETHODS M M physical conditions in the tidal zones are quite different; the higher shore is wetted Study site almost exclusively by tidal sea level rise, but the lower shore receives considerable wave The study was carried out on the intertidal action. rocky shore of Ohoiwait (latitude 5045’15” S, longitude 132057’20” E), Big Kai Island,

5°18' ∗N

Banda Sea 5°26'

5°34'

5°46' Ohoiwait

5°54' S Arafura Sea E

132°34' 132°42' 132°50'132°58'

Fig 1. Map of study site of Ohoiwait located at the Big Kai Island.

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Journal of Coastal Deveolpment ISSN : 1410-5217 Volume 11, Number 2, February 2008 : 89-96

Population structure or other exudates. U is assumed to be negligibly small, and is ignored in this Population of Cellana testudinaria was study. A is the energy flow through, or studied at the rocky shore of Ohoiwait, energy assimilated by the population. where previous work had been done on the Ideally, all components of the energy distribution, abundance, and biomass of this budgets should be estimated separately species (Khouw, 2006b). The rocky shore of (Paine, 1971), to provide internal checks on Ohoiwait, described in detail by Khouw their reliability. However, due to the nature (2003), is exposed to prevailing south- of feeding, it was impossible to estimate C. northly monsoons, therefore, the perpetual restudinaria separately, and there were no “dry” season which is characterized of daily data available for an independent estimate of maximum insolation and minimum humidity mortality (E). An approximation was, and precipitation. therefore, made by assuming steady-state Density of species varied enormously, conditions and stable size-frequency even within short distance (10 m), along the structures of population. Steady growth rates shore. Topography seemed to be the main and continuous spawning throughout the cause of this heterogeneity. Population year perhaps lessen the error involved in samples were taken from small areas of these assumptions. Under steady-state shore having a fairly uniform topography. condition ∆B = 0 so that Pg = E. i.e., the Acquisition of data sufficient for population estimate of production due to growth and estimates over larger areas of shoreline was recruitment (Pg) is assumed to equal the beyond the scope of this study. C. mortality (E). testudinaria occupied a well defined zone, which was sampled throughout its 25 m Production (P) 2 wide range by six 1 m continuous quadrats Growth (Pg) forming a square with sides of 3 m. The equation used to estimate the annual -K(t – Energy Budget growth in shell length was Lt = L∞ [1 – e to) ] where Lt is the length at age t, L∞ is the The population energy budget may be asymptotic length, K is the growth represented by the equation: C = P + R + F coefficient, and t0 is the theoretical age at + U where P = Pg + Pr, Pg = ∆B + E, and P length 0 (Bertalanffy von, 1938). + R = A. The terminology is that The relationship between shell length recommended by Chislett (1969). All the and ash free dry weight (AFDW) was found components may be expressed as by extracting from their shell, Kcal/m2/year. C is the total amount of removing the heavy calcareous operculum, energy consumed by the population; drying for 48 hours at 70 oC and weighing to production (P) comprises energy added to 0.1 mg. Regression equation with 95% the population by growth and recruitment confidence limits fitted to the data is: ln (Pg), and the energy released as spawned AFDW = ln a + b ln shell length. gametes (Pr). Pg is also equal to the sum of Calorimetric determination was made ∆B, the net increase or decrease in the by burning three approximately 1 g standing stock of the population, and E, the replicates, of the powdered tissue of the energy eliminated from the population due species, dried for 48 hours at 70 oC in an to mortality. R is the metabolic heat loss adiabatic bomb calorimeter (Parr Instrument from the population, estimated from rates of Company, Illinois, USA). Ash contents were oxygen consumption. F is the energy lost via estimated by roasting the samples at 600 oC the faeces and U is the energy lost via urine in a muffle furnace for 12 h. The calorific 91

Journal of Coastal Deveolpment ISSN : 1410-5217 Volume 11, Number 2, February 2008 : 89-96

value of C. testudinaria (21.59 Kcal/g each respirometer were kept in the AFDW) was used to convert growth in respiration chambers for 1 hour before biomass to energy increments (Pg). commencing the experiments. The means of 4 consecutive hourly readings were taken, Spawning (Pr) and the shell length of limpet measured to the nearest 0.1 mm. C. testudinaria deposite their egg capsules on the rocks about mean tide level (MTL). Defaecation (F) Egg capsules tend to be laid in shallow water-filled depressions, underneath rocks, Limpets collected at dawn were placed on or where irregularities in the rock surface native rock in glass fingerbowls in the afford some protection from the sun. laboratory. Seawater came to a level For the purpose of computing Pr, halfway up the rock, and a perspex cover Khouw (2003) figures 150 egg capsules/year prevented individuals from escaping. Faecal for an “average” sized C. testudinaria was pellets were collected 24 hrs later, briefly used. According to Khouw’s size-frequency washed in tap water to remove sea salt, dried data, the length of the average sexually for 24 hrs at 70 oC, and weighed to 0.1 mg. mature individual was 30 mm. Shell lengths of the limpets were measured To determine calorific value, C. to 0.1 mm. Equation with 95 % confidence testudinaria egg capsules were carefully limits relating faecal production scraped from building bricks on which they (mg/limpet/24 hrs) to shell length (mm): Ln had been laid, and examined for rupture of dry weight faeces = Ln shell length + a. the lower wall. Only intact capsules were Calorific values of faeces were used (about 25%). The calorific value of estimated by wet oxidation with potassium four replicates, each of 20 capsules, was iodate in sulphuric acid. Energy lost as estimated by wet oxidation with potassium faeces (F) from the population was iodate in sulphuric acid. The mean with 95% estimated from size-frequency data, the confidence limits was 4.41 ± 0.36 relationship between rate of faecal cal/capsule. production and size, and the calorific values. Gonad weight, and hence gamete production, was assumed to be a function of the cube of the shell length. On this assumption, the calories produced per RESULTS AND DISCUSSION animal per year as gametes may be expressed as a function of shell length (mm) Results by the following equation: Ln gamete Population Structure production = 3*ln shell length – a. The size class structure of the population of Respiration (R) C. testudinaria was studied through the analysis of percentage size frequency Limpets collected from the field were kept distribution (Fig. 2). The 2402 collected in running seawater at about 30 oC specimens ranged in length from 8.2 to 31.8 overnight, during which time they voided mm with an average of 16.22 ± 5.26 mm most of the faeces. Scholander manometric while their total body wet weight varied respirometers manufactured by (the Mark between 0.11 and 4.93 g with an average of Company, Randolph, Massechusset, USA) 0.55 ± 0.70 g (Khouw, 2007). were placed in a constant-temperature bath The distribution was markedly at 30.4 ± 0.05 oC. Sets of 10 limpets, one in bimodal (2 cohorts), with a greater excess of 92

Journal of Coastal Deveolpment ISSN : 1410-5217 Volume 11, Number 2, February 2008 : 89-96

the larger density at the small size group C. testudinaria population was due to (12.5 – 14.5 mm) and a slight excess of the growth conditions, or whether the sub- smaller density at the big size group (24.5 – population (cohort) after some previous 26.5 mm). Since limpets could not be aged, increasing in size was in phase of recovery it is impossible to say whether the and would eventually resemble the other differences in size-frequency structure of the sub-population.

20

18 16 14 12 10 8

6 4 2 0 8.5 9.5 10.5 11.5 12.5 13.5 14.5 15.5 16.5 17.5 18.5 19.5 20.5 21.5 22.5 23.5 24.5 25.5 26.5 27.5 28.5 29.5 30.5 31.5 Mean length (mm)

Fig 2. Cellana testudinaria. Mean percentage frequency of each size class category. Vertical lines represent standard deviation

Growth (Pg) Spawning (Pr)

The von Bertalanffy equation of C. Using Khouw (2007) figures, a 25.80 mm testudinaria (Khouw, 2007) used to estimate female C. testudinaria and the relationship the annual growth in shell length was Lt = equation of Ln gamete production = 3 ln 33.08 [1 – e-1.4(t + 0.09)]. From this equation, shell length – 4.4642 (Khouw, 2003) was the shell length of limpet at the age of 1 year estimated to produce 197.73 cal/year. The old is 25.80 mm. The 95 % confidence calorific value (Pr), therefore, was estimated limits of the relationship between shell to be 0.87 Kcal/m2/year. Summing the length and total body wet weight for the values for Pg and Pr, the figures for total whole period of study was WW = production, P, is 2.42 Kcal/m2/year. 0.0002343(± 0.000031) L2.6601(± 0.0454) (Fig. 3), hence 95 % confidence limits of the Respiration (R) relationship between ash-free dry weight (mg AFDW) and total body wet weight (mg Energy lost as heat from the population due WW) was AFDW = 0.03236(± 0.0178) WW to metabolism was estimated from 2.7703(± 0.3813) (Khouw, 2006b). It was, respiration rates measured in the laboratory. therefore, found that the calorific value (Pg) Oxygen consumption rate was converted to of C. testudinaria was 1.55 Kcal/m2/year. heat production by multiplying by an oxycalorie coefficient which assumes that, when carbohydrate fat and protein are 93

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completely burned in 1 ml of oxygen at O2/ind./hr = 0.7206 ln wet flesh weight normal temperature and pressure (NTP), an (WW) + 0.1569. The mean respiration rates, average of 4.89 cal are released (Sutherland, therefore, obtained in this study was 217.3 1972; Wright & Hartnoll, 1981; Workman, Kcal/m2/year. 1983). The appropriate equation: Ln µl

5 4.5 4 3.5 3 2.5 2 1.5 1 0.5 0 7 1217222732

Fig 3. Cellana testudinaria. Relationship between shell length

(L) and total body wet weight (WW) (Khouw, 2006b).

Pg + Pr = 1.55 + 2.42 = 3.97, (2) A = P + R = Defaecation (F) 3.97 + 217.3 = 221.27, and (3) C = A + F = 221.27 + 351.4 = 572.67. The proportion of Regression fitted to the data suggest that energy assimilated which is lost via faecal production is roughly proportional to metabolism (R/A x 100%) is 98%, the the square of the shell length. Equation with assimilation efficiency (A/C x 100%) is 95% confidence limits relating faecal 39%, the net growth efficiency (P/A x production (g/limpet/24 hr) to shell length 100%) is 1.8%, and the ecological efficiency (mm) is: Ln dry weight faeces/ind./24 hrs = (E/C x 100%) is 0.3%. 1.6950 (± 0.3584) ln shell length – 3.9989 (± 0.3178). The 95% confidence limits of Discussion calorific value of the faeces, therefore, were estimated by wet oxidation with potassium Compared with many other invertebrates iodate in sulphuric acid to be 287.1 (± 25.5) (Sutherland, 1972; Picken, 1980; Parry, cal/g. Energy lost as faeces (F) from the 1982; Workman, 1983; Blankley & Branch, population was estimated to be 351.4 1985), the Cellana testudinaria is estimated Kcal/m2/year. to lose a high percentage of assimilated energy via metabolism. A similarly high Energy Budget estimate of assimilated energy lost via metabolism (95%) was given by Wright & Summation of the components estimated Hartnoll (1981) for vulgata, which is above complete the population energy also an intertidal gastropod browsing on budget in Kcal/m2/year as follows: (1) P = detritus and algae.

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Williams & Morritt (1995) suggested ONCLUSION that long live poikilotherms, where a C proportion of the population is in excess of two years old, lose more of assimilated This study establishes a baseline for energy via heat loss. Such are ecological energetics of Cellana testudinaria supposed to experience high respiratory living on the rocky shore of Ohoiwait. Large cost, non-productive periods, e.g. Cellana differences in population structure, and grata, during summer at lower latitudes or hence population energetics of this species during aestivation, so that annual production occurred at different zones along the shore. efficiencies are low. Limpet C. testudinaria The proportion of assimilated energy lost via species falls into this category. metabolism was rather high (98%) but Net growth efficiency of C. comparable to the intertidal limpet Patella testudinaria was relatively low (other vulgata (95%) studied by Wright & Hartnoll invertebrates range from 11 to 73 %; (1981). Assimilation efficiency (39%) was Branch, 1981), and may have been due to higher but net growth efficiency (1.8%) was slight underestimations of growth rates by lower compared to others intertidal limpets von Bertalanffy equation. In general, there is 11-73% studied by Branch (1981), while a strong positive correlation between growth ecological energetics was 0.3%. and production. Somatic growth (Pg) can be reduced in favor of reproductive effort (Pr), as it has been showed by Branch (1981) for ACKNOWLEDGEMENTS seven South African Patella species.

However, overall the growth rate was Personally I would like to address my thanks positively correlated with the reproductive to Vonny Litamahuputty and Winfield effort. This implies that although energy Bierhoff Khouw, my wife and son, for their may be diverted from P to P (or vice versa) g r tremendous patience, support and guidance when food is short, in general species have throughout this study. A special thank to “strategies” of high or low turnover (Branch, Julius Notanubun, my student and colleague, 1981). who facilitated this research by providing The assessment of the energy content field equipment and technical during field calculated for the limpet C. testudinaria, experiment. gives a value of 21.59 kJ.g-1 AFDW. This value was considerably higher than that of many temperate limpet species, such as (19.3 kJ.g-1 AFDW) REFERENCES (Workman, 1983), and Nacella delesserti (20 kJ.g-1) (Blankley & Branch, 1985), but Bertalanffy L. Von., 1938. A quantitatif eventually similar to the tropical limpet theory of organic growth (inquiries on species such as (22.59 growth laws–II). Hum. Biol.,10 : 181- kJ.g-1), Notoacmaea petterdi (21.63 kJ.g-1), 213. Patella peroni (22.30 kJ.g-1), and alticostata (22.93 kJ.g-1) (Parry, 1982). An Blankley, W.O. & G.M. Branch., 1985. attempt to present the species energy Ecology of the limpet Nacella budgets in a more useful way was made by delesserti (Philippi) at Marion Island expressing production (P), assimilation or in the Sub-Antartic southern ocean. J. energy flow (A) and total energy Exp. Mar. Biol. Ecol., 92 : 259-281. consumption (C) as functions of animal size. Branch, G.M., 1981. The biology of limpets: 95

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physical factors, energy flow and Southeast Moluccas, Indonesia. Indon ecological interactions. Oceanogr. J. Mar. Sci. 11, (4) : 181-192. Mar. Biol. Annu. Rev., 19: 235-380. Khouw, A.S., 2007. Growth determination Chislett, G.R., 1969. Comparative aspects of of tropical limpet Cellana the ecology of three Nerita (: testudinaria (Linnaeus, 1758) living ) species from different on the rocky shore of Ohoiwait, locations in Barbados. Unpublished Southeast Moluccas, Indonesia. J. MSc. Thesis: McGill University. Coast.Dev.10, (2) : 89-103.

Khouw, A.S., 2002. Growth pattern and Paine, R.T., 1971. Energy flow in a natural shell shape variation exhibited by population of the herbivorous intertidal limpets in relation to their gastropod Tegula funebralis. Limnol. zonal distribution. Ichthyos. 1: 1-11. Oceanogr., 16 : 86-98.

Khouw, A.S., 2003. Ecological studies on Parry, G.D., 1982. Evolution of the life- the tropical limpet Cellana histories of four species of intertidal testudinaria (Linnaeus, 1758): limpet. Ecol. Monogr., 52 : 65-92. Influence of environmental factors on the rocky shore benthos of the big Kai Picken, G.B., 1980. The distribution, growth Island, Southeast Moluccas, and reproduction of the Antarctic Indonesia. Unpublished Dr.rer.nat. limpet Nacella (Patinigera) concinna Dissertation: Aus dem Institut (Strebel 1908). J. Exp. Mar. Biol. für Polarökologie der Christian- Ecol., 42 : 71-85. Albrechts-Universität zu Kiel. Sutherland, J.P., 1972. Energetics of high Khouw, A.S., 2005. Recruitment pattern of and low population of the limpet tropical limpet Cellana testudinaria scabra (Gould). Ecology. 53 : (Class: Gastropoda, Family: 430-437. ) living on the rocky shore of Ohoiwait, Southeast Moluccas, Williams, G.A., & D. Morritt., 1995. Habitat Indonesia. Indon J. Mar. Sci. 10, (3) : partitioning and thermal tolerance in a 135-142. tropical limpet . Mar. Ecol. Prog. Ser. 124 : 89-103. Khouw, A.S., 2006a. Productivity of tropical limpet Cellana testudinaria (Linnaeus, Workman, C., 1983. Comparisons of Energy 1758) living on the rocky shore of Partitioning in contrasting Age- Ohoiwait, Southeast Moluccas, Structured Populations of the Limpet Indonesia. J. Cost. Dev. 9, (2) : 119- Patella vulgata L. J. Exp. Mar. Biol. 127. Ecol., 68, (1) : 81-103.

Khouw, A. S., 2006b. Distriution, Wright, J.R., & R.G. Hartnoll., 1981. An abundance, and biomass of tropical energy budget for a population of the limpet Cellana testudinaria (Class: limpet Patella vulgata. J. Mar. Biol. Gastropoda, Family: Patellidae) living Ass. U.K., 61 : 627-646. on the rocky shore of Ohoiwait,

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N

5°18' ∗

Banda Sea 5°26'

5°34'

5°46' Ohoiwait

5°54'

Arafura Sea S 132°34' 132°42' 132°50' 132°58' E

Figure 1. Map of study site of Ohoiwait located at the Big Kai Island.

20

18

16 14 12

10

8 6 4

(%) Frequency Percentage 2

0

Mean length (mm)

Figure 2. Cellana testudinaria. Mean percentage frequency of each size class category. Vertical lines represent98 standard deviation (SD).

Journal of Coastal Deveolpment ISSN : 1410-5217 Volume 11, Number 2, February 2008 : 89-96

5 4.5 4 3.5 3

2.5 2 1.5 1 Total body wet weight (g) 0.5

0 7 1217222732 Shell length (mm) Figure 3. Cellana testudinaria. Relationship between shell length (L) and total body wet weight (WW) (Khouw, 2006b).

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