Energetics of the limpet Lottia kogamogai (Gastropoda: Acmaeidae) in an intertidal rocky shore in southern Hokkaido, Japan

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<ul><li><p>LJournal of Experimental Marine Biology and Ecology,224 (1998) 167181</p><p>Energetics of the limpet Lottia kogamogai (Gastropoda:Acmaeidae) in an intertidal rocky shore in southern</p><p>Hokkaido, Japana , b b*Cui-Juan Niu , Shigeru Nakao , Seiji Goshima</p><p>aDepartment of Biology, Beijing Normal University, Beijing 100875, ChinabLaboratory of Mariculture, Faculty of Fisheries, Hokkaido University, 041 Hakodate, Japan</p><p>Received 21 March 1997; received in revised form 14 July 1997; accepted 19 July 1997</p><p>Abstract</p><p>We investigated, at both individual and population levels, the energy budget of a small limpet,Lottia kogamogai, which is a numerically dominant species in intertidal areas of Usujiri, southernHokkaido, Japan. Annual energy consumption was estimated to be 0.20, 1.42, 3.06, 4.75, 5.85 and</p><p>21 216.97 kJ year ind. for 05 year old limpets, respectively. Assimilation efficiency was 65.9%.Of the assimilated energy, a major proportion was used for mucus secretion and the proportionincreased distinctly with age, from 40% in 0 year animals to 80% in individuals over 3 years old.Metabolic loss of assimilated energy declined from 30% in 0 year old animals to 15% in limpetsover 3 years old. Energy loss due to ammonia excretion is negligible, accounting for less than0.5% of consumption. Growth efficiencies of 05 year old individuals were 19.0, 7.7, 4.7, 3.0, 2.8</p><p>22and 2.3%, respectively. In one year, approximately 434 kJ m energy flowed through the</p><p>22population, of which about 147 kJ m was defecated as faeces. The energy allocated to growth22</p><p>and reproduction was relatively low, only 24.7 kJ m , while that expended for mucus secretion22 22</p><p>and metabolism were 206.7 kJ m and 55.4 kJ m , respectively. The population had a P/B ratioof 1.67. The net growth efficiency, gross growth efficiency and ecological efficiency were 8.6%,5.7% and 4.6%, respectively. 1998 Elsevier Science B.V.</p><p>Keywords: Limpet; Lottia kogamogai; Energetics; Mucus</p><p>1. Introduction</p><p>Intertidal limpets are major grazers and play an important role in the transfer ofenergy in intertidal rocky shore ecosystems (Wright and Hartnoll, 1981; Hawkins and</p><p>*Correspondence author. Tel.: 186 10 62207720; fax: 186 10 6220056; e-mail: cjniu@bnu.edu.cn</p><p>0022-0981/98/$19.00 1998 Elsevier Science B.V. All rights reserved.PII S0022-0981( 97 )00190-1</p></li><li><p>168 C. Niu et al. / J. Exp. Mar. Biol. Ecol. 224 (1998) 167 181</p><p>Hartnoll, 1983), and they are well suited for energetic studies (Creese, 1981). Severalbioenergetic studies on intertidal limpet populations have been published (Branch,1981). However, most of the energy budgets established for limpet populations haveomitted the energy lost by mucus secretion (see Branch, 1981, for a review) despite itrepresents a considerable proportion of the assimilated energy (Davies et al., 1990,1992). Furthermore, studies on mucus production have been primarily on largegastropod grazers (Horn, 1986; Davies et al., 1990; Kideys and Hartnoll, 1991). In thisstudy, an energy budget was determined for a natural population of the small limpetLottia kogamogai (previously known as Collisella heroldi Dunker, Sasaki and Okutani,1994). L. kogamogai is widely distributed from southern Hokkaido to Taiwan and isnumerically dominant in the macrobenthos of many intertidal rocky shore communities.Previously, we have reported the reproductive cycle, growth pattern, distribution,population structure, mortality and the production of L. kogamogai individuals andpopulation as a whole, as well as the energy requirement for metabolism at thepopulation level (Niu and Fuji, 1989; Niu et al., 1992, 1994a,b, 1997). Now in thisreport, we have constructed comprehensive energy budgets for L. kogamogai, at bothindividual and population levels, with particular attention to energy lost by mucusproduction.</p><p>2. Materials and methods</p><p>The study area was an intertidal rocky shore in Usujiri, Southern Hokkaido, Japan(42821N, 140857E). Detailed information about the study site and sampling stations aregiven in Fuji and Nomura (1990); Niu et al. (1992). Among the components of astandard energy budget C 5 P 1 R 1 M 1 F 1 U (C: consumption; P: production; R:energy losses through metabolism; M: mucal losses; F : faecal losses; and U : excretion),we have previously reported results for P and R for L. kogamogai (Niu et al., 1994b,1997). Below are methods for measuring the other components.</p><p>2.1. Measuring mucal losses</p><p>Every two months, from August 1990 to August 1991, limpets were collectedrandomly from the whole study area at day-time low tide, and immediately brought tothe laboratory for the mucus secretion experiment. The foot of each animal was carefullyscraped free of mucus and washed with sea water to clean of faeces and other debris.About 1020 healthy limpets with different body sizes were selected for the experiment.Every animal was then placed inside a plastic box laden with clean thin coverglass plateson the bottom and the surrounding walls. The initial position of the animal was marked.To assess mucus secretion in water, these plastic boxes were immersed in fresh seawater. The limpets were observed to be very mobile whilst immersed. After about 6 h,the animal was removed from the glass and distance between the final and initialposition was measured. Every limpet was then cleaned of its foot, and the coverglassesin each box were dried. To assess mucus secretion in air, formerly immersed animalswere placed inside the same plastic box with new coverglasses but without sea water.</p></li><li><p>C. Niu et al. / J. Exp. Mar. Biol. Ecol. 224 (1998) 167 181 169</p><p>The box was covered to maintain certain humidity. Almost all the limpets did not moveunder this condition. Again the experiment lasted for about 6 h, simulating the meantime of immersion or air-exposure by the tide at MTL. Control glass plates were set upduring both experiments.</p><p>After the experiment, sample coverglasses with dried mucus were broken into finepieces. Then, caloric content of the glass pieces was measured using the iodate-sulfuricacid wet-oxidation method described in detail by Karzinkin and Tarkovskaya (1960);Hughes (1969). The caloric content of the experimental glass plates in each plastic boxwas assumed to be the energy of the mucus secreted by the experimental limpet. At theend of the experiments, shell-free dry body weights were measured for all experimentallimpets. They were dried at 608C and then weighed with an electrical balance to 0.1 mgaccuracy.</p><p>In sea water, the limpets were very mobile, and the mucus was used for both adhesion21 21 21</p><p>and movement. Mucus secretion rate was expressed by the unit J h cm ind. . Toutilize these laboratory data to assess mucus production in the field, regression equationsof mucus secretion rate versus shell-free body dry weight were calculated for each 2month sample. Assuming mucus secretion rates were the same in laboratory and in thefield, the energy costs of mucus secretion for individuals in each age group duringimmersion in one tidal cycle in the field was calculated using the regression equations;the travelled distance data by limpets in the field; the immersion time data shown in Niuet al. (1997) (Table 1), and the data of mean shell-free dry body weights of each agegroup in every month (Fig. 1 in Niu et al., 1994b). The energy of mucus sample duringemersion was often too low to be measured, so limpets with similar body weights werepooled. Because the limpets were stationary without sea water, mucus secretion rate was</p><p>21 21expressed by the unit J h ind. under this situation. Probably because of small samplesizes, no significant correlations were found between mucus secretion rates and shell-free dry body weights (regression analysis: p . 0.05) during emersion. Thus, the age ofexperimental limpets was determined by the method in Niu et al. (1992), and meanmucus secretion rates were calculated for each age group in every season (means with nosignificant differences were pooled). Likewise, the energy costs during emersion time inone tidal cycle were also calculated for each age group using the emersion time datashown in Niu et al. (1997) (Table 1).</p><p>Every month during the study period, 4050 animals in the field were uniquelymarked using numbered dymal-tape adhered onto their shells during day time low tide.Their initial positions were also marked with matching dymal-tapes adhered on the rock.After one tidal cycle, the marked limpets were searched for, and the straight-linedistances between their final and initial positions were measured.</p><p>2.2. Measuring ammonia excretion</p><p>The principal excretory product in molluscs is generally ammonia (Barkai andGriffiths, 1988); therefore, only the excretory loss in the form of ammonia wasmeasured. Ammonia excretion rate was determined under ambient sea-water tempera-tures. Ten to twenty animals with various body weights were placed into plastic jarsfilled with known volumes of filtered sea water. After 610 h, the ammonia level in the</p></li><li><p>170 C. Niu et al. / J. Exp. Mar. Biol. Ecol. 224 (1998) 167 181</p><p>experimental sea water samples and three controls was measured by the Strichlandmethod. The difference in ammonia level between the sample and the control sea waterwas used to determine the ammonia excreted by the limpet. The energy cost of excretion</p><p>21was estimated by using the conversion factor of 22.98 J mg of ammonia (Holdwayand Beamish, 1984). Shell-free dry body weights were determined for the experimentallimpets using the method mentioned earlier. Regression equations of ammonia excretionrate versus shell-free dry body weight were calculated for each month. Assumingammonia was excreted only during immersion, the daily energy costs of ammoniaexcretion for individuals in each age group in the field was calculated using theregression equations; the immersion time data shown in Niu et al. (1997) (Table 1), andthe data of mean shell-free dry body weights of each age group in every month (Fig. 1 inNiu et al., 1994b).</p><p>2.3. Measuring assimilation efficiency, consumption and faecal output</p><p>Laboratory feeding experiments showed that L. kogamogai grazed everything onpolycarbonate plates coated with a film of microflora and detritus. Microscopicexamination showed that the algal film on the plate was mainly comprised of diatoms.Thus, we used the indirect method for measuring assimilation efficiency, as described inCrisp (1989), using ash as the indicator. Limpets collected monthly from the field werereared in the laboratory on polycarbonate plates which had previously been immersed insea water and become covered by an obvious algal-film. Tidal rhythm was simulatedduring the rearing experiment. After at least 3 days of rearing, when it was certain thatthe limpets had ejected all faeces coming from feeding in the field, collection of faeceswas started by hanging the plates with limpets on them inside an aquarium filled withsea water. Faeces were collected daily with a siphon pipe, washed with diluted water anddried at 608C to a constant weight. The ash content of the faeces was determined byburning them at 5008C for 4 h while the caloric content was measured using thewet-oxidation method. Dry weights, ash and calorific contents of the algal food oncontrol plates were also measured at the same time. Assimilation efficiency (AE) wascalculated using the following equation:</p><p>AE 5 (F 2 E) /((1 2 E) 3 F )) 3 100%</p><p>Where F5ash-free dry weight of the food/ food dry weight; E5ash-free dry weight ofthe faeces / faeces dry weight.</p><p>Assuming AE was similar in the field and in laboratory conditions, C and F of limpetsin the field were calculated by the following equations:</p><p>C 2 F 5 P 1 R 1 U 1 M and AE 5 (C 2 F ) /C</p><p>On the basis of the individual energy budgets and data for the population dynamics of L.kogamogai (Niu et al., 1992, 1994a), we assessed the annual energy flow of a L.kogamogai population.</p></li><li><p>C. Niu et al. / J. Exp. Mar. Biol. Ecol. 224 (1998) 167 181 171</p><p>Table 121 21 21L. kogamogai: Bimonthly relationships between mucus secretion rate (J h cm ind. ) in water, and body</p><p>dry weight (mg)Month Equation n r p</p><p>Dec. and Jan. log M51.199 log W22.720 14 0.80 ,0.05Feb. and Mar. log M50.737 log W21.390 14 0.52 ,0.05Apr. and May log M51.385 log W22.716 17 0.68 ,0.05Jun. and Jul. log M51.542 log W22.913 10 0.90 ,0.05Aug. and Sep. log M50.688 log W22.033 19 0.58 ,0.05Oct. and Nov. log M50.713 log W22.442 10 0.72 ,0.05</p><p>3. Results</p><p>3.1. Mucus production</p><p>Table 1 shows the regression equations of mucus secretion rate during immersion,versus shell-free body dry weight, while Table 2 shows the seasonal mucus secretionrates of each age group during emersion. There are significant differences among theseequations (Anocova: p,0.001). Mean distances travelled by limpets in the field duringone tidal cycle were 4.9365.30, 1.6861.98, 2.5964.99, 7.3869.81, 8.7269.51,8.6166.22, 5.6765.20, 5.2464.55, 8.97610.59, 29.44617.06, 14.05616.53,8.48612.02 cm for JanuaryDecember, respectively. The animals moved less inFebruary and March, and travelled significantly further in October and November than inother months (Anova: p,0.05). Fig. 1 shows the seasonal changes of mucus secretionfor individuals of different ages.</p><p>3.2. Ammonia excretion</p><p>Comparison of the regression equations representing the relationship between21 21</p><p>ammonia excretion rate (N: mg-at.NH4 h ind. ) and shell-free dry body weight (W :mg) for each month revealed no significant difference (Anocova: df511, 118; F50.6710; p.0.5). Therefore, a pooled equation was calculated as:</p><p>LogN 5 0.5957logW 2 2.3432 (r 5 0.58, n 5 130, p , 0.001)</p><p>Table 221 21L. kogamogai: Seasonal mean mucus secretion rate (J h ind. ) in air by different age groups</p><p>Season Age group</p><p>0 year 1 year 2 year 3 year 4 year 5 year</p><p>Spring 0 0.005 0.018 0.031 0.122 0.233Summer 0 0.102 0.254 0.157 0.256 0.328Autumn 0 0.070 0.084 0.359 0.213 0.311Winter 0 0 0.106 0.221 0.325 0.325</p></li><li><p>172 C. Niu et al. / J. Exp. Mar. Biol. Ecol. 224 (1998) 167 181</p><p>21 21Fig. 1. L. kogamogai: Daily energy cost of mucus secretion (J ind day ) in every month by individuals indifferent age groups.</p><p>21 21Fig. 2. L. kogamogai: Daily energy cost of ammonia excretion (J ind day ) in every month by individualsin different age groups.</p></li><li><p>C. Niu et al. / J. Exp. Mar. Biol. Ecol. 224 (1998) 167 181 173</p><p>Fig. 2 shows the seasonal changes in daily energy costs of ammonia excretion forindividuals of different ages.</p><p>3.3. Assimilation efficiency, consumption and faecal ejection</p><p>Table 3 shows the energy contents of the food and the faeces of the limpets measuredin the laboratory. No significant seasonal difference was found in the energy content ofthe faeces ( p.0.05). On the other hand, the energy content of the food showed adistinct increase from June to August. Monthly assimilation efficiencies, AEs, showedno significant differences ( p.0.05) among different age groups of L. kogamogai,indicating that AE is independent of the age of the animal. Thus, assimilationefficiencies for every month with all age groups pooled were calculated and the resultsare...</p></li></ul>