MARINE ECOLOGY PROGRESS SERIES Vol. 36: 139-149, 1987 - Published March 2 Mar. Ecol. Prog. Ser.

Population dynamics of Capitellacapitata (Polychaeta; Capitellidae) in an organically polluted cove

Hiroaki Tsutsumi

Amakusa Marine BiologicalLaboratory. KyushuUniversity, Tomioka. Reihoku-cho, Amakusa. Kumamoto-ken,Japan 863-25

ABSTRACT: The population dynamics of a sibling species of CapiteUa capitata (Fabricius) in a cove organically polluted by fish farrn~ngwere characterized by early recolonizahon m azoic areas, very rapid population growth, and extinction following development of extremely anaerobic conditions during summer. The remarkably high potential for population growth results from the short life cycle and continual reproduction as a population. Previously, the production of planktonic larvae with the ability to disperse over a wide area was considered one of the most important life history characteristics of opportunistic polychaetes in unpredictable habitats. In the present study, however, Capitella sp. exhibited opportunistic population dynamics during benthic recovery after defaunation in heavily polluted areas, despite production of a small number of large eggs with restricted dispersal ability via lecithotrophic larvae. The size cornposibon of the recolonizing population suggested that some of the worms were recruited as mature adults from a very small population maintalned in the immediate vicinity of the sampling station in an environment disturbed by organic pollution. Although the populahon dynamics of Capitella sp. appear to be characteristic of highly opportunisbc organisms, results suggest that populations may be maintained within each habitat by reliance only on a remarkably large potential for population growth. In general, organically polluted areas may not be temporary habitats that Capitella sp. can utilize only during benthic recovery immediately after defaunation, but rather such areas may be their native habitats.

INTRODUCTION nated conditions often results in temporary defauna- tion, only the predominant polychaetes, C. capitata The general distribution of benthic macrofauna and and the spionid polychaetes, can recolonize azoic sediments along a gradient of organic enrichment has areas quickly and restore their populations to their been revealed by benthic studies of organically earlier slzes in a short period of time during the process polluted areas over the past 2 decades (Kitamori 1975, of benthic fauna1 recovery after defaunation (Kolmel Pearson & Rosenberg 1976, 1978, Reish 1979). Benthic 1979, Yamamoto 1981, Tsutsumi & Kikuchi 1983). C. communities in the most polluted areas are not diverse. capitata is not more tolerant of extreme hypoxia than Only a few species of small polychaetes Capitella the dominant species in semi-healthy zones (Reish capitata and some spionids (Scolelepsis fuliginosa, 1966) or in less polluted areas (Ueno & Yamamoto Paraprionospio pinnata, Polydora Ligni etc.), predomi- 1982). In recent years, the exclusive domination of C. nate. In particular, C. capitata occurs at high densities capitata in organically polluted areas has been recog- only in heavily polluted areas throughout the world nized to be a reflection of its life history characteristics, (Reish 1971, 1979, Rosenberg 1972, 1976, Wade et al. in particular its adaption to unpredictable environ- 1972, Halcrow et al. 1973, Grassle & Grassle 1974, ments, rather than of its tolerance of hypoxia (Warren Pearson & Rosenberg 1978, Yamamoto 1980, Tsutsurni 1984). & lkuchi 1983). Bottom water and sediment in organi- The rapid recovery of Capitella capitata after cally polluted areas are apt to become anaerobic in environmental disturbance has also been reported in a summer, because of accelerated decomposition of follow-up study of benthic communities seriously dam- abundant organic matter and stagnation of the bottom aged by an oil spill (Grassle & Grassle 1974). McCall water. Although the occurrence of extremely deoxyge- (1977) indicated that C. capitata, together with the

O Inter-Research/Printed in F. R. Germany 140 Mar. Ecol. Prog. Ser. 36. 13CL149, 1987

spionid polychaete Streblospio benedicti, recolonized and the evolutionary implications of such characteris- early in experimental boxes of azoic sediments. Thus, tics. early recolonization and rapid population growth are I have studied seasonal fluctuations of the benthic notable life history characteristics of C. capitata in communities and the life history and populabon disturbed habitats, and are propehes similar to those dynamics of a Capitella species in a cove, Tomoe Cove, of other opportunistic species (Grassle & Grassle 1974, organically polluted by fish farming in Arnakusa, 1976, McCall 1977). South Japan, since 1978 (Tsutsumi 1983, Tsutsumi & However, studies of the life history of Capitella Kikuchi 1983, 1984). Field and laboratory studies on capitata (Wu 1964, Bellan et al. 1972, Foret 1974, Reish Capitella sp, indicate a constancy in the size of mature 1974, Grassle & Grassle 1976, Warren 1976a, Kkuchi eggs throughout the year, and no marked changes in 1979, Yamamoto 1980, Tsutsumi & Kikuchi 1984, brood size per female that cannot be accounted for by unpubl.), electrophoretic analysis (Grassle & Grassle concommitant changes in the body size of brooding 1976), and chromosomal studies (Grassle et al. in females. I have, therefore, concluded that a single press), have indicated that this species actually con- species of Capitella is represented in the population in sists of numerous sibling species, with similar adult the present study area, and it is referred to here as morphologies but distinct reproductive modes, that Capitella capitata. In general, the features of its life generally occur in different geographic regions, but history closely resemble those of Capitella sp. I which occasionally occur sympatncally (Grassle & Grassle has the most rapid response following environmental 1976, 1977). Their characteristics differ greatly; the disturbance (Grassle & Grassle 1976, Grassle 1980). differences in colonizing abhty among the sibling The aims of the present study were to analyse the species reflect differences in the environmental varia- population dynamics of Capitella capitata in the bility of their respective habitats (Grassle 1980). organically polluted cove, and to elucidate the Hence, there is only a Limited number of species in the mechanisms that contribute to the rapid growth of the whole sibling species complex of C. capitata that occur population after recolonization, and those that allow in disturbed habitats and which exhibit highly oppor- this species to maintain its population in the cove with tunistic properhes. the environmental conditions disturbed by organic en- Life history strategies of Capitella species that occur richment. in disturbed habitats have been studied in the last I also investigated the population dynamics of decade. Early studies (Grassle & Grassle 1974, McCall Capitella capitata on the muddy flat, Shioiri Flat, adja- 1977) categorized the life history strategies of these cent to Tomoe Cove. Here, samples of C, capitata were sibling species as opportunistic (or r-strategist, as collected throughout the year, although seasonal fluc- defined by Wilson & Bossert 1971) or fugitive (sensu tuations in population density are quite large (Tsut- Gadgil & Solbrig 1972) etc. The term 'fugitive (oppor- sumi 1983). These results will be reported elsewhere. tunistic)' stresses the ability of planktonic larvae to disperse over a wide area, one of the most important STUDY AREA life history characteristics of the Capitella species which allows them to discover open, short-lived, Tomoe Cove is a subsidiary cove of Tomioka Bay habitats and to establish a population quickly. Recent whlch is located on the northwestern corner of Ama- life history studies, however, have shown that these kusa Shimoshima Island, on the west coast of Kyushu, sibling species produce few large eggs, and have Japan (32O32' N, 130°02' E) (Fig. la). The cove is semi- rather limited abhty to dsperse by means of pelagic enclosed by a narrow sand spit and the mouth of the lecithotrophic larvae. Furthermore, other species of cove is shallower than the cove itself. Thus, the influ- Capitella, which produce many small eggs and have ence of Bay water on the cove is minimal. Seasonal the greatest powers of larval dispersal, in fact occur in variation in bottom water temperature in the cove was less variable habitats (Grassle & Grassle 1976, 1977, from about 12.g°C in February to 24.g°C in August 1978, Grassle 1980, Tsutsurni & Kkuchi 1983). The (Fig. 2). Fish farming is camed out in the eastern part relationship between the life history characteristics of of the cove (hatched area in Fig. la, b). Red sea bream the sibling species of CapiteUa and the predictability Pagrus major are reared in floating net cages and fed of environmental conditions in their habitats con- with anchovies. Fish faeces and uneaten food residues tradicts predictions made by models of life history disperse, or sink to the bottom, resulting in a large strategy. Apparently, descripbons of the life history organic contribution to the bottom water and sediment strategies of Capitella species that occur in disturbed of the cove. Depletion of dissolved oxygen occurs in habitats require revision, which may also help to eluci- the cove bottom water every summer, because of date life history characteristics of other marine inver- increased degradation of organic matter and limited tebrates that are favored in unstable environments, water renewal. Tsutsumi: Population dynamics of Capitella capjtata 141

Fig. 1.Study area, Kyushu, Japan. (a) Topography and bathy- metry. (b) Locations of sampling stations in Tomoe Cove: (m) stations where the distribution of Capitella capitata was studied; (0) station (Stn T) used for the population study. Hatched areas: cages used in fish farming; open rectangles: unused cages; dark areas: intertidal zone

from November 1979 to April 1980, and 4 to 6 times per month from May 1980 to February 1981. At Stn T, samples of bottom water, for measurement of dissolved oxygen, and samples of surface sediment, for measure- ment of total sulphide, were taken 2 to 5 times per month from May to December 1980. Dissolved oxygen was measured by Winkler's method; total sulphide was determined using an H2S absorbent column tube ('Hedorotec', Kitazawa Sangyo Co. Ltd.). Sediments in the present study area were classified Sediment samples were taken with an Ekman-Birge by their silt-clay content (The Meteorological Agency bottom sampler (20 cm X 20 cm) from a boat. Four grab of Japan 1970). The bottom sediment of Tomoe Cove samples were collected at each station in the survey on could be separated into 3 types based on grain size: (1) 1 May 1979. Samples were sieved on 1.0 mm mesh a homogeneous mud bottom (silt-clay content of the screen on the boat, and the residues were fixed in a sediment > 75 %) inside the cove; (2) a sandy mud (silt- 10 '10 formalin solution containing Rose Bengal. During clay content 50 to 75 %); and (3) a muddy sand bottom sampling on 17 May, 22 August, and 23 September (silt-clay content between 25 and 50 '10). The sandy 1980, at least 3 grab samples were taken at each mud and muddy sand were found at the mouth and outside the cove.

MATERIALS AND METHODS

The abundance of Capitellacapitata was estimated at 10 sampling stations in Tomoe Cove (Fig. la) on 1 May 1979 and at 23 stations around the floating cages used for fish farming in the eastern part of the cove (Fig. lb) on 17 May, 22 August, and 23 September 1980. One of these stations, Stn T, located inside the fish farm, was selected for the population study. Sam- Fig. 2. Seasonal temperature variations in bottom water at Stn ples were taken at fortnightly or monthly intervals T, Tomoe Cove 142 Mar. Ecol. Prog. Ser. 36: 139-149, 1987

station, and 5 subsamples were collected from each of MAY 13,1980 them with a small corer (6.25 cm X 6.25 cm X 5 cm). The sediment samples were brought back to the laboratory, fixed in a 10 % formalin solution containing Rose Bengal, and sieved on 0.5 mm mesh screen. Samplings at Stn T were carried out in almost the same manner as that described above, but 10 to 20 subsam- ples were prepared on each occasion, and sieved on 0.125 mm fine mesh screen. Since Capitella capitata juveniles just after settlement have a body size between 0.14 and 0.16 mm in thoracic width, all of the specimens in the samples should be retained on the 0.125 mm mesh screen. The worms were sorted and counted under a stereomicroscope and preserved in 10 % formalin solution. The sex of adult worms was determined by examina- tion of the morphology of the notosetae in the 8th and 9th thoracic setigers. The maximum thoracic width of Capitella capitata was taken as the measure of body size since it is closely correlated with dry body weight (Tsutsumi & Kikuchi 1984). Thoracic setigers are stout and were never injured during samphng and proces- sing. Specimens were placed under a stereomicro- scope equipped with a camera lucida, and their mag- Fig. 4. CapiteUa capitata. Distribution (ind 0.01 m-2) around nified images (30 X) projected onto paper set under the the fish farming cages (hatched areas) in Tomoe Cove on 13 camera lucida. The maximum thoracic widths (usually May 1980. (Samples sieved on a 0.5 mm screen). (0) Station (Stn T) used in the population study the 5th or 6th setiger is widest) of the projected images were recorded as 2 pin holes on the paper. The distan- ces between the pin holes were measured by a graphic digitizer (Gradimate, Oscon) connected to a micro- computer (Multi 16, Mitsubishi Electric Co.), and the actual maximum thoracic widths of the specimens were calculated and stored on floppy disc. Analysis of the generation structure of the Capitella capitata population was also performed using a com- puter. The size-frequency distribution of the popula- tion was calculated from the body size data stored on the floppy disc, and the results were plotted by compu- ter. Polymodal distributions of size frequency were divided into monomodal ones by a modified version of the graphic methods of Cassie (1954) and Taylor (1965), programmed in Basic 86 (Tsutsumi unpubl.).

RESULTS

Distribution and abundance

The study of the Capitella capitata population in Tomoe Cove has been in progress since 1979. The cove has been organically polluted by fish farming for the past decade. Fig. 3 shows the abundance of C. capitata (ind 0.16m-~)at 10 sampling stations in the cove on 1 Fig. 3. Capitella capjtata. Distribution (ind 0.16m-2) in Tomoe May 1979. The highest densities occurred at the most Cove on 1 May 1979. Hatched areas: cages used in fish organically polluted stations, adjacent to the source of iarm~ng.(Samples sieved on a 1.0 mm screen) the organic discharge. Tsutsurn~:Populat~on dynamics of Capitella capitata 143

Distribution of this dense population was investi- at Stn T fluctuated throughout the summer but gener- gated in more detail in spring 1980, since benthic ally remained below 1 m1 1-' from July to September. communities in the cove tend to become most abun- Large amounts of total sulphides, including hydrogen dant in spring (Tsutsumi & Ktkuchi 1983). Fig. 4 shows sulphide, accumulated in the sediment following the the abundance of Capitella capitata at 23 stations depletion of dissolved oxygen (Fig. 6). The dense around the floatlng cages on 13 May 1980. The highest population of CapiteUa capitata in the heady polluted densities (> 25 000 m-2) were found in the immediately area disappeared in July and the organisms did not vicinity of the fish farming cages, i.e. the source of begin to re-establish themselves until late October polluhon, but quickly diminished at stations a short when the concentration of dissolved oxygen increased, distance away. and the sulphide content of the sediment began to fall. Seasonal fluctuations in population density at Stn T A survey of 23 stations around the fish farming cages are shown in Fig. 5. The highest density in 1980 (about (Fig. lb) on 22 August and 23 September 1980 revealed 47 000 m-2) was recorded in May. The population had no C. capitata. Additionally, 28 stations in the cove completely disappeared by July, when conditions on were sampled in mid-July 1981 and 8 stations in the the bottom became extremely reduced (Fig. 6). The cove were sampled in mid-July 1985. During both concentration of dissolved oxygen in the bottom water summers, no specimens of C. capitata were found. When C. capitata recolonized Stn T in October 1980 (Fig. 5), the population showed a remarkably high potential for growth, reaching a density of more than 50 000 m-' within 3 mo.

Size composition of a recolonizing population

Sampling at Stn T, at approximately weekly inter- vals, was carried out from May to December 1980 to determine the population dynamics of Capitella capitata. No specimens were found up to and including 3 October, since extinction of the population in mid- June. Recolonization by C. capitata was first observed in samples taken on 12 October. Changes in the size NDJFMAMJ JASONDJFM '79 '80 '81 distribution at Stn T are shown in Fig. 7. Recoloniza- Fig. 5. CapiteLla capitata. Seasonal fluctuations of density tion was indicated by the discovery of a single brood- (ind 0.01m-2, ? 2 SD, n = 10) at Stn T, Tomoe Cove. (Samples ing female (a female brooding embryos in a brood sieved on a 0.125 mm screen) tube) in one of a total of 20 cores (800 cm2). On 21 October, 73 juvenile worms were found with 3 adults (one brooding female and 2 fully mature males) in 20 cores. It is noteworthy that some adult worms were included in the colonizing population. Extremely anaerobic conditions in the bottom water and sediment persisted until late September at this station (Fig. 6). It is therefore probable that these adult worms did not migrate to the site of recolonization as planktonic lar- vae. Capitella capitata is a sedentary polychaete with limited mobhty. The worms burrow slowly through the sediment. Although no remnants of the population were discovered during the summer within several hundred meters of the fish farm, in spite of intensive sampling, the presence of adult worms in the recol- MJJASOND onizing population at Stn T suggests that a very small '80 population was maintained throughout the summer Fig. 6. Measurements of the concentration of chssolved oxy- somewhere close to this station. It is possible that the gen (D. 0.)in the bottom water and total sulphide content (T. S.) in the sediment at Stn T, Tomoe Cove, during the summer first recruits at Stn T (73 juveniles) collected on 21 stratification period October (Fig. 7) may have been derived from the larvae 144 Mar. Ecol. Prog. Ser. 36: 139-149, 1987

1980 OCT 12 OCT 21 OCT 28 NOV 06 NOV 12 NOV 25 E 1.5 N=1 1.5 1.61 N=418 1.6 N=446 E I I I N=368 l

2 01 001 0- 0L-- 0- 100(%1 5 10 15 20(%) 5 10 16(%1 6 10 15(%) 5 10 16(%) 6 10 15 20(%) FREQUENCY

1980 DEC 04 DEC 10 DEC 16 DEC 22 DEC 30 1.6r N=277 1.5, N=411 1.6, N=497 1.6, N=818 N=660

010- 0+ 0- 0- 5 10 15(%) 5 10 15(%) 5 10 15 20(%) 5 10 15 20 25(%) 5 10 15 20 25(%) FREQUENCY Fig. 7. Capitella capitata. Size-frequency distributions of the recolonizing population. Filled bars: brooding females

and 400 larvae. Such relatively small brood sizes may M BRWDlNG FEMALE M NON - BROOD1NG be too small to compensate for the larval loss that MATURE FEMALE accompanies widespread dispersal at the larval pelagic stage. The timing of reproduction in the CapiteUa capitata population appears to be synchronous with spring tide. Fig. 8 shows the densities of brooding and non-brood- ing females, and the lunar cycle from October to December 1980. The density of brooding females reached a peak twice during these 3 months (on 6 Nov and 10 Dec), although the second peak was less pro- nounced. Both in the laboratory colonies and in the field populations, almost all of the females which were brooding larvae in their brood tubes had ripened ovanes in their abdominal segments, although no ovanes were observed in the females just after spawn- MOON +O- e- 0-0- 0- ing embryos into the brood tubes. These reproductive Fig. 8. CapiteLla capitata. Monthly density fluctuations of characteristics indicated that the ovaries of females brooding females and non-brooding mature females, Oct to matured a second time during the brooding period for Dec 1980 only about 1 wk to 10 d, suggesting that females have the potential to reproduce at least twice. However, in in the brood tubes of these surviving adults. Brooding the laboratory, females reproduced only once and died females with thoracic widths of more than 1.0 mm, soon after they had finished brooding (Tsutsumi & collected on 12 and 21 October, produced between 300 Kikuchl 1984). In the present follow-up study, female Tsutsumi: Population dynamics of Capitella capitata 145

mortality after brooding in the field population was analysed with the data on synchronous reproduction shown in Fig. 8. As mentioned above, females can mature their ovaries during the brooding period again. Therefore, the females emerging from brood tubes after brooding also should have mature ovaries, and be regarded as non-brooding mature females. Here, if female mortal- ity after brooding was minor, the decrease in the density of brooding females caused by the finish of brooding would be followed by an increase in the density of non-brooding mature females. The changes in the density of non-brooding mature females, how- ever, preceded or were synchronized with those of brooding females in the field population (Fig. 8). Thus, Fig. 9. Capitella capitata. Changes of modes in size-fre- female mortality after brooding is considered also to be quency distributions of each cohort. Numbers designate the very high in the field population. In the present study, cohorts described in the text. (0) Presence of brooding females the Capitella capitata population reproduced syn- and mature males in the cohort chronously twice from October to December. Since fe- male mortality after brooding is considered to be very some fully mature adults were also included in this high, few females that contributed to the first peak of cohort. Cohort 3 completed its life cycle out of phase synchronous reproduction would have survived until with the cycles of Cohorts 2 and 4. Cohort 3 recruited the second peak occurred. These 2 synchronous repro- between 12 and 21 October, and grew to about 0.85 ductions therefore appear to be caused by 2 different mm (mode) in thoracic width on 4 December. The groups of mature females. synchronous reproduction of this cohort resulted in the The synchronous reproduction in the Capitella second peak in the density of brooding females on 10 capitata population resulted in the synchronous December (Fig. 8), when Cohort 5 was produced. recruitment of members to the size class at settlement Cohort 3 also took 6 wk to complete its life cycle, and (mostly to the class of 0.15 to 0.20 mm) thoracic width disappeared by the end of December. Thus, in the immediately after the density of brooding females had present study area, the population of Capitellacapitata reached its peak. Very many recruits were observed in consisted of 2 cohorts with short and monotelic life the size-frequency distnbutions on 12 November and cycles. The one was being recruited into the estab- 10 December (Fig. 7).These newly formed peaks in the lished population while the other had already fully distribution have been treated as representative of a matured. Both juveniles immediately after settlement succession of cohorts. and mature adults were, therefore, often found in the Growth of each cohort was followed by tracing the population simultaneously. changes of the modes in the size-frequency curves. In the present study, 4 cohorts were produced during the 3 mo from October to December (Fig. 9). Generation DISCUSSION structure changes during this period were interpreted as follows, considering high female mortality after The population of Capitella capitatawas made up of brooding and synchronous reproduction in the popula- 2 cohorts with a short, monotelic life cycle, each repro- tion. ducing synchronously (Fig. 9). Consequently, repro- Cohort 2 matured with a thoracic width of about 1.0 duction and mass recruitment were frequently mm (mode) at the beginning of November, and pro- observed, and brooding females and juveniles, just duced Cohort 4, which recruited from 12 to 25 after settlement, were collected on almost every sampl- November. The first peak in the density of brooding ing occasion (Fig. 7 & 8). This type of generation females on 6 November (Fig. 8) resulted from the structure and these reproductive characteristics were synchronous reproduction of Cohort 2. Almost all also observed in the population of C. capitata on females and males of this cohort appeared to die soon Shioiri Flat adjacent to Tomoe Cove (Fig. 1) (Tsutsumi after their first reproduction. It was already difficult to 1983). Since both populations of C. capitata reproduce detect the size-frequency dstribution of Cohort 2 in throughout almost the whole year (Tsutsumi & Kikuchi the population when Cohort 4 was recruiting. Cohort 4 1984), it is probable that the 2 cohorts that make up grew to about 1.0 mm (mode) in thoracic width by 30 each population of C. capitata repeat monotelic, short December, only about 6 wk after its settlement, and life cycles throughout the year. Thus, the potential for 146 Mar. Ecol. Prog. Ser. 36: 139-149, 1987

population growth of C. capitata is considerably higher early winter. It maintained its high population than that of many other annual or perennial benthic densities until total defaunation occurred again during animals that are found in more stable habitats and that the early part of the following summer, in spite of have relatively long prereproductive periods. subsequent recolonization by other polychaetes and The generation structure of Capitella capitata, made bivalves (Tsutsumi & lkuchi 1983, present study). The up of 2 cohorts, has never previously been reported in population dynamics of Capitella species established population studies of Capitella species. Earlier studies in organically polluted areas may be stable as long as were, however, based on only monthly or biweekly environmental conditions remain aerobic, even if other samplings (Grassle & Grassle 1974, Warren 1976b, benthic animals coexist with them. Oyenekan 1980, Chesney & Tenore 1985), which make A series of laboratory experiments by Tenore using it very difficult to analyse the reproductive cycle and Capitella sp. I, which has, apparently, the most oppor- generation structure of species with such a short life tunistic life history (Grassle & Grassle 1976), clearly cycle. Since a long breeding season, extending almost demonstrated the nutritional control of individual throughout the year, and early maturation are common growth rates, population sizes and annual production life history characteristics among Capitella species (Tenore 1977, 1981, 1983). Although the population found in habitats disturbed by organic pollution in size of this species osc~llated cyclically during long- various geographic regions (Reish 1961, 1974, Foret term experiments over approximately 2 yr, the size of 1974, Grassle & Grassle 1976, Grassle 1980, Yamamoto laboratory populations consistently reflected the nutn- 1981, Tsutsumi & lkuchi 1984), the rapid growth of tiona! leve!s avdable (Chesney & Tenore 1985, Capitella populations reported from other localities Tenore & Chesney 1985). Such a relationship between may also be caused by the same mechanisms as those nutritional conditions and some population parameters observed in the present study. of the Capitella species was also supported by the The concentration of Capitella sp. populations in laboratory experiments with Capitella capitata occur- organically polluted areas as shown in Fig. 3 & 4 has ring in the present study area, using azoic sediments previously been considered to be a reflection of the with various levels of organic matter (unpubl. data, opportunistic characteristics of their life histories results to be reported elsewhere). The body size of (Grassle & Grassle 1974, Rosenberg 1976, Pearson & females at the time when they reproduced varied con- Rosenberg 1978). Grassle & Grassle (1974) adopted the siderably, depending on nutritional conditions during definition of r-strategist proposed by Wilson & Bossert the prereproductive period. Juveniles reared with (1971) as that of an opportunist adapted for life in a organically polluted sediments from just below the fish short-lived, unpredictable habitat by relylng on a high farm grew into fdy mature adults of approximately r to make use of ephemeral resources. In a new habitat the same size as those in the field population after 1 mo such a species would: '(1) discover the habitat quickly, in the laboratory, while juveniles fed on less polluted (2) reproduce rapidly to use up the resources before sediments collected from areas away from the fish farm other, competing, species could exploit the habitat, did not even attain the body size (about 0.5 mm in and (3) disperse in search of other new habitats as the thoracic width) at which they commenced sexual mat- existing one began to grow unfavourable' (Wilson & uration, or else they only reached the minimum adult Bossert 1971). The population dynamics of the body size and produced just a few eggs, after 1 mo. Capitella species reported by Grassle & Grassle (1974). Therefore, it appears that the absence of Capitella sp. Rosenberg (1976), and McCall (1977) was, in fact, in less organically polluted areas with stable environ- characterized by early recolonization of azoic areas, mental conditions, and the rapid decline of their popu- rapid population growth immediately after recoloniza- lation~in the benthic recovery process that follows the tion, and rapid decline in population sizes during the regression of pollution, can be ascribed to the shortage recovery process of other fauna. These characteristics of organic intake and to their physiological demand for appeared to support the hypothetical opportunism of organic matter rather than to their poor ability to com- these Capitella species. However, it is uncertain pete with other benthic animals considered to be less whether a biological interaction alone was responsible opportunistic. The physiological requirement for large for the rapid decline in the population sizes of the amounts of organic matter to maintain individual Capitella species, because faunal replacement was growth and population size may concentrate the dis- followed by regression of organic pollution. tribution of the Capitella species exclusively in heady In the process of faunal recovery after defaunation of polluted areas. the present study area, Capitella capitata recolonized The early recolonlzation of infaunal polychaetes, azoic areas adjacent to the fish farming cages, where a such as some Capitella species and spionid large amount of organic matter was continuously dis- polychaetes with limited adult mob~lltyin azoic areas, charged by the farming activities, from late autumn to has been previously considered to arise from the pro- Tsutsumi: Population dymamics of Capitella capitata 147

duction of planktonic larvae with the abhty to dis- K-selection (Stearns 1976, Southwood 1977, Begon & perse over a large area (Grassle & Grassle 1974, Mortimer 1981) and opportunism (Grassle & Grassle ffikuchi & Tanaka 1976, McCall 1977, ffikuchi 1979, 1974, McCall 1977), and the characteristics of environ- Santos & Simon 1980). However, Capitella species, in mental disturbances that actually occur in organically fact, produce lecithotrophic larvae with rather short polluted areas. Dispersal or migratory strategies have planktonic stages that range from several hours to 1 d been mainly seen as adaptations to environmental (Grassle & Grassle 1976, Grassle 1980, Tsutsumi & deterioration occurring randomly in time and space. Kikuchi 1984). Although Capitella species occurring in On the other hand, in the present study, Capitella organically polluted areas show the most rapid capitata in the organically polluted areas suffers from response to environmental variability, their reproduc- extremely deoxygenated bottom conditions which pre- tive modes and processes of larval development indi- vail over the whole area in which it is distributed from cate that they possess limited ability to disperse by summer to early autumn, and remnants of these popu- means of planktonic larvae. lation~persisting throughout the summer have never The results of the present study suggest that a very been discovered in grab samplings from the cove. The small population of CapiteUa capitata persists some- extremely reduced environments would be, therefore, where adjacent to the heavily polluted area in the cove a seasonal rather than randomly occurring adversity throughout the summer. Although such a refugial for C, capitata. The life history of this polychaete does population was never discovered in summer, the size- not, however, include a period of diapause (or dor- frequency distributions of the Capitella population mancy) like that observed among plants and animals shortly after recolonization involved not only newly- that occur in environments subject to seasonal adver- settled recruits but also some adult worms (Fig. ?). sity (Stearns 1976, Begon & Mortimer 1981). It seems These adult worms must be derived from a population unlikely that the early recolonization by Capitella sp. persisting in organically enriched areas near the fish in the process of fauna1 recovery after defaunation is farm throughout the summer. Their presence indicates directly associated with opportunistic life history that this species did not necessarily recolonize the area strategies which stress widespread dispersal by means solely by means of planktonic larvae. Furthermore, of planktonic larvae or dispersive strategies like those colonization by a considerable number of C. capitata suggested in previous studies on life history strategy. was sometimes found in a vessel containing sediment, Recent studies on Capitella species indicate a rela- hung about 1 m above the bottom under the floating tion between these species and the reduced conditions fish cages in summer (unpubl. data). I observed that that tend to occur in organically enriched bottom sedi- these worms emerged from the sediment and crawled ments. Cuomo (1985) demonstrated that larval settle- up the inner sides of the bottle when conditions ment of Capitella sp. I was promoted by sulphides, became anaerobic. At the fish farm, a large number of which are naturally occurring products of the ropes were stretched along the bottom to anchor the anaerobic decomposition of organic matter, both in the floating cages. If juvenile or adult C. capitata can laboratory and under semi-natural conditions. Warren climb up the ropes to a level 1 m above the bottom, or if (1984) showed that a Capitella species not only has an the larvae during their short pelagic period can settle aerobic metabolic pathway but also an anaerobic one. in the sediment that accumulates among the barnacles CapiteLla species with a high potential for population attached to the ropes, a small population could remain growth and poor dispersal (or migratory) ability, occur- under relatively aerobic conditions during the sum- ring in organically polluted areas, may be regarded as mer. Three adult C. capitata were actually collected organisms that positively select moderately reduced from small ropes which had been set along the main sediments as their habitats. That is, the organically ropes of the floating cages for 2 wk in October 1980. polluted areas may not be temporary habitats that Therefore, it seems likely that recolonization of the some Capitella species can utilize only during the bottom in the immediately vicinity of the fish cages did process of benthic recovery immediately after defauna- not depend on the ability of C. capitata to disperse its tion, but rather such areas may be their native habitats. larvae widely, but depended rather on the presence of Future studies on population dynamics and physiology a very small population that had taken refuge in the of the Capitella species will clarify further the reasons less anaerobic conditions prevailing on the fish cages for their association with organically polluted areas. ropes, a meter or so above the bottom. Such seed populations would not be detected by routine benthic Acknowledgements. I heartily thank Prof. T. fikuchi, Dr. M. sampling. Tanaka, and Dr. S. Nojima for their innumerable suggestions, and Dr. J. P. Grassle for her critical comments, suggestions We should note the differences between the charac- and improvements of the English text. I also thank Dr. A. M. teristics of the unpredictable environment assumed in Kijrner and Mr. R. K. Nakamura for their improvements of the the theories of life history strategy, especially in r- and English text. I am indebted to Messrs I. Goto and T. Samejima 148 Mar. Ecol. Prog. Ser. 36: 139-149, 1987

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Ths article was presented by Professor T. Fenchel; it was accepted for printing on December 23, 1986