Ontogenetic changes in individual growth and egestion rates in the deposit-feeding polychaete Capitella sp. 1

J. Exp. Mar. Bial. Ecol., 1990, Vol. 143, pp. 209-220 Elsevier

209

JEMBE 01504

Ontogenetic changes in individual growth and egestion rates in the deposit-feeding polychaete Capitella sp. 1 Thomas L. Forbes and Glenn R. Lopez Marine Sciences Research Center, State University of New York at Stony Brook, Stony Brook, New York, USA

(Received 8 March 1990; revision received 17 August 1990; accepted 17 August 1990) Abstract: Repeated measurements of indi~dual worms over a 28-d period were used to calculated volumespeciiic growth (G) and egestion rates at a high, constant food ration (11000 mg N. m - 2 ’ d‘ ’ ). Worm sizes ranged from 0.1-9.0 mm3 body volume (BV) (=20-1600 pg dry weight (DW)), 1.8-18.7 mm live body length). The relationship between G and BV was highly variable but displayed a plateau at sizes between

0.5-3.5 mm’ (120-830 pg OW) where G remained in the range of 18-20x d- i. In contrast to predictions of empirical growth models, G did not show a monotonic decrease with increasing worm volume. individual volume-specific egestion rates (V,, = mm3 sediment egested. (mm3 worm)- 1. d _ ‘) showed an analogous but Iess broad peak at z 2 mm’ BV, suggesting a functional coupling between specific egestion and growth rates. No relationships were found between G and sex or G and body size. G was also independent of the total volume or mass of sediment processed for time lags of up to 28 d. G increased linearly as a function of V,, up to specific egestion rates of 2.7 mm3 sediment egested I (mm’ worm)- ’ d - ‘. With further increases in V,,, growth rates remained constant at 25%. d-l. BV was positively related to cumulative egestion (mm3 sediment egested) with an average female reaching sexuai maturity after egestion of = 20 mm3 of sediment. Increased variability in meas~ements of gross individual production efliciency for the smallest animals (GPE = G ’ (mm3 sediment egested) ’ ,100) suggests that the efficiency of energy transfer from ingested food to tissue in smaller worms ($1 mm3) may be much more sensitive to environmental or physiological influences. Smaller worms experience both greater growth and degrowth per unit egested sediment than larger worms. The increased variability of GPE in smaller animals may be due to a lack of stored energy reserves in combination with the interaction between absolute body size and the scale of distribution of the sedimentary food resource. Key words: Capitella; Egestion rate; Growth rate

INTRODUCTION

The reIationship between energy intake and growth is central to an underst~ding of animal bioenergetics (e.g. Calow & Townsend, 1981; Sibly & Calow, 1986). Recent studies of the deposit-feeding CapitelIa species group have focused on the effect of food ration on important population-level parameters (Tenore, 1981, 1983; Tenore et al., 1982; Tenore & Chesney, 198.5; Chesney, 1985; Chesney & Tenore, 1985; Gremare

Correspondence address: T. L. Forbes, Biology Institute, Odense University, Campusvej 55,5230 Odense M, Denmark. 0022-0981/90/$03.50 0 1990 Elsevier Science Publishers B.V. (Biomedical Division)

T.L. FORBES AND G.R. LOPEZ

210

et al., 1988; 1989a; 1989b). For example, processes

such as population

fluctuations

have

of food or nitrogen

egestion

rate measurements rates are relatively

culture

on

However,

rate because

defined

ration

and biomass of sediment

study egestion

under

capacity, conditions.

feeding

determined

the influence

rate, system carrying

measurements of the growth responses of individual animals as a function processing rates at constant food rations have not been made. In the present

been

production

have been used as a measure easy to measure

of

and, for deposit-

feeders, they constitute a very accurate surrogate measure of the amount of particulate material ingested per unit time. This is a consequence of the predominance of an indigestible, mineral-grain fraction in sedimentary deposits (Lopez & Levinton, 1987). Given the fundamental energetic importance of egestion to growth and development, the detailed study of ontogenetic changes in growth and egestion rates of individual animals is a prerequisite to an increase in our understanding of the factors that may affect growth rates in nature. The purpose of this study was to complete a detailed investigation of the ontogeny of growth and egestion rates in individual animals from early postsettlement

juveniles

to large adults.

MATERIALS AND METHODS GROWTH ESTIMATES AND GENERAL PROTOCOL Ten worms were grown individually in small (12.6 cm’) glass dishes. Growth rates were estimated from 2-d growth intervals. Living animals were sized and all pellets egested by each worm were collected and counted every 2 d for 3 wk. Natural sediment enriched with Gerber’s mixed cereal was also changed every 2 d to maintain a constant ration as described below. Volume-specific growth rates (G) (% volume change. individual’ * d- ‘) were calculated following Kaufmann (1981): G (% .d-‘)

= {[ln(BI’r) - ln(BV,)/d]}.

where BV, = final worm volume

100,

(mm3), BV, = initial worm volume (mm’).

Calculations of G were based on a 4-d growth interval to ensure a measurable change in size. G and V,, were then plotted against geometric mean body volume (GMV): GMI’=

[(BP’&. (SF’,)]“’

to relate growth to body size. These calculations were based on the assumption that worms were cylindrical in shape, and body volumes were estimated as described previously (Forbes, 1989b; Forbes & Lopez, 1987).

GROWTH EGESTION

AND

GROWTH

AND

EGESTION

IN Cz4PITELLA

211

EXPERIMENT

The egestion and growth rate measurements began with individuals ranging in initial size from 0.1 to 1 mm3 and were made every 2 d for 28 d. The experiment began with 10 individuals, one animal per dish. Volume-specific egestion rate (mm’ sediment egested . (mm3 worm) - l. d - I ( If,,)) was calculated by dividing the total volume of sediment egested in 2 d by the GA4V for that interval. Experimental temperature and salinity were maintained at 15 + 0.5 “C and 28.0&, respectively. Animals were fed a mixture of silt-clay sediment (< 63 pm, 10% AFDW) that was enriched with an amount of Gerber’s mixed cereal chosen to ensure that the worms were not nitrogen-limited. Sediment prepared in this manner provided a daily nitrogen rationof > 1000mgN~m-2~d-‘. Ret en t work indicated that worm growth rates were positively related to nitrogen ration using Gerber’s mixed cereal (Tenore & Chesney, 1985; Marsh et al., 1989). However, ratios of nitrogen daily ration to nitrogen standing biomass of worms (g N * d- ’ ration per g N worms, (R : B)) greater than z 0.4-l did not increase growth rates. The R: B ratios used for the present experiments were between 10 (for large worms) and 800 (for the smallest worms) and thus should have maximised growth with respect to nitrogen in the experimental system. The addition of cereal to the sediment was low enough to ensure that the fecal pellets produced by the worms were natural in appearance (i.e. compact and robust) and were identical in dimensions to pellets produced on 100% natural sediments. Fecal pellet volume was estimated from pellet length and width measurements. Pellets were assumed to be ellipsoidal in shape and their volumes calculated as ellipsoids of revolution (Protter & Morrey, 1964). STATISTICAL

ANALYSES

Due to the great variability of the data, scatterplots were examined for trends using a robust, locally weighted scatterplot smoother {see Cleveland, 1979; Cleveland & McGill, 1984 for a thorough discussion of the methodology) and moving regression analyses (Brown et al., 1975; Forbes, 1989a; Forbes & Lopez, 1989). These methods allow exploration of bivariate data plots without a priori assumptions about the functional nature of the relationships. Changes in the variance or “spread” of G and V,, as functions of body volume were analyzed using spread smoothings of the G and V,, scatterplots as outlined in Cleveland & McGill (1984). Thus the smoothed values of the absolute residuals are robust, locally weighted estimates of the spread or variance in Y (G or V,,) for a given value of X (B V), RESULTS

Growth and egestion rate measurements were made for worms ranging in body volume from 0.1 to 9 mm3 GMV (X = 1.79, SD = 1.871, N = 86), and thus covered a

212

T.L. FORBES

0

1

AND G.R. LOPEZ

2

3

4

5

6

7

Mean Worm Volume (mm3) Fig. 1. Changes in volume-specific growth rate (G) (% volume change (mm3).dm ‘) as a function of geometric mean worm volume [(BP, .BVr)IR] for each 4-d growth interval. Curve is a LOWESS middle smoothing (Cleveland, 1979).

90-fold increase in size during development. Developmental stages ranged from early postsettlement juveniles to sexually mature adults. This range of body volumes corresponds to dry weights (DW) of ~20-1600 pg (conversion factors between wet weight, D W, carbon and nitrogen content are given in Cammen (1985) and Marsh et al. (1989)). Mean G for all worms over all growth intervals was 15.35% ad-’ (SD = 8.437, range = - 4.13 to 38.20% * d- ‘, N = 86). For the pooled data there was no correlation

cl

2

4

6

6

10

Mean Worm Volume (mm3) Fig. 2. Changes in volume-specific egestion rate (mm3 sediment egested.(mm’ worm)- ’ ‘d- ‘) as a function of geometric mean worm volume [(BP,. BV,)‘“] for each 2-d growth interval. Curve is a LOWESS middle smoothing (Cleveland, 1979).

GROWTH AND EGESTION IN C.4PITELL.4

Volume-speczflc

Egestion

213

Rate

Fig. 3. Plot of volume-spe~i~c growth rate (G) (% volume change (mm”) *d _ ‘) as a function of volumespecific egestion rate (F,,) (mm’ sediment egested . (mm’ worm) _ ’ . d ’ ) for each 2-d growth interval. Where G = 10.135 * V,, - 3.253; for V,, I 2.7 and G = 24.608 for V,, > 2.7. Error sum of squares = 16,166 (N = 85). See text and Nickerson et al. (1989) for computational details.

between G and worm size (mm’) (P = 0.1273, IV = 77 (4-d growth interval) (Fig. 1). However, scatterplot smoothing analysis of the G vs. GMV data suggested a size-dependent trend with maximum growth rates occurring at B V values between 0.5 and 3 mm3 with peak G values of z 17-18x * d- ’ (Fig. 1). The smoothing of the I/,,vs. GMV data showed an analogous but less broad peak at RC2 mm3 BV with worms between 1 and 2 mm3 BY egesting more than twice their body volume per day (Fig. 2). Both scatterplot smoothing and moving regression analyses suggested a two-phase linear relationship between G and V,, (see Methods). Thus in order to predict growth rates as a function of specific egestion rates we have fitted a two-piece least-squares model to the data (Nickerson et al., 1989) (Fig. 3). This model indicates that G increased linearly with increasing V,, up to values of 2.7 mm3 sediment egested * (mm” worm)- ’ * d - I. The slope of the second phase was not significantly different from zero (FUSS= 0.415, 0.50 -=IP < 0.75). Therefore a reduced model was fitted to the data (Nickerson et al., 1989). The reduced model indicated that at V,, values > 2.7, G was constant at 25 y0 - d- 1 ,^ tb

-

m 10.00

a-1

G

c

=oXd-~

G

:

=z5x

=m?d-’ =l@Xd-’ =5Xd-l

c

l 3

i

1.00

L2 38 0.10:

IH 0.02

M

W

0.04

.‘.‘I

“’

0.10

Mean Worm

1.00

Volume

10.00

(mm3)

Fig. 4. Plot of egestion rate (mm3 sediment egested . d- ‘) vs. geometric mean worm volume. Isopleths are predicted growth rates based on measured specific egestion rates (total sediment egested over growth interval (mm’)) and the fitted relationship between G and V,,.

214

T’.L. FORBES

AND G. R. LOPEZ

Fig. 5. Plot of absolute value of the egestion rate residuals vs. geometric mean worm volume. The smooth curve is a spread smoothing of the absolute value of the residuals of the fitted curve for V,, vs. GMV (Fig. 2). See text for computational details.

The growth-rate isopleths on the daily egestion rate (mm3 +d - ‘) vs. B V plot (Fig. 4) were calculated using two empirical reIationships: (1) the previously described ontogenetic relationship between egestion rate (volume sediment egested/time) and body size (Forbes, 1989a; Forbes & Lopez, 1989) and (2) the fitted two-phase relationship between G and V,, (Fig. 3). The apparent narrowing of the spread of log egestion rate values as a function of log BV suggested that the lowest variability in predicted G may

0

1

2

3

4

5

6

7

Mean Worm Volume (mm3) Fig. 6. Plot of the absolute value of the growth rate residuals vs. geometric mean worm volume. The smooth curve is a spread smoothing of the absolute value of the residuals of the &ted curve for G vs. GMV (Fig. I). See text for computational details.

215

GROWTH AND EGESTION IN CAPIZ’ELLA

Cumulative

Egestion

(mrn3)

Fig. 7. Plot of geometric mean worm volume vs. cumulative egestion (mm3).

have occurred in worms between % 1 and 2 mm3 BV (note the conspicuous absence of points below predicted growth rates of 10y0 * d - ’ at B V between 0.8 and 3 mm3, Fig. 4). A more detailed analysis of the distribution of the absolute values of the residuals about the fitted smoothing of V,. vs. body volume confirmed that this was indeed the case, at least for worms <4 mm’ BP’. This is indicated by the spread smoothing of V,, as a function of BV which reached minimum values at BV values between 1 and 2 mm3 (Fig. 5). An analogous minimum spread in the G values was indicated by the smoothing of the absolute residuals from the fitted line between G and BV (Fig. 6). This size region of low variance in V,, and G as a function of BP’ occurs at worm sizes where V,,. and G reach maximum values (cf. Figs. 1, 2, 4). There was a positive relationship between cumulative egestion (mm’ total sediment egested) and B i/ (Fig. 7). The spread of worm sizes as a function of cumulative egestion also appears to increase as worms grow to sizes greater than x 2.5 mm3 ( = 30 mm3 sediment egested) (Fig. 7). However, G was not related to the total volume of sediment processed over the 4-d growth measurement periods (r = 0.088, hJ = 84).

30

75 ,

Mean Worm Volume (mm3)

Mean Worm Volume

(mm3)

Fig. 8. (a) Plot of gross production efhciency (G&Y) (growth (mm3).(mm~ sediment egestedf- ’ ] vs. geometric mean worm volume. See text for method of curve calculation. (b) Plot of predicted gross production efficiency (GI%,)minus measured gross production efficiency (GPE,) as a function ofgeometric mean worm volume.

T.L. FORBES AND G.R. LOPEZ

216

TABLE

I

ANCOVA

of volume-specific growth rate (C) as a function of individual worm and worm body size. Where GMV = geometric mean body volume (mm3). The nonsignificant interaction term was removed. ANCOVA

Source

ss

Worm GMV Error

df

MS

F ratio

P

0.453 2.588

0.885 0.112

875.036 625.021

8 1

109.379 625.021

17 869.928

14

241.486

ANCOVA revealed no differences in G (2-d growth intervals) among the individual worms, where each sex was represented by at least two individuals (Table I). However, this result should be interpreted with caution for two reasons: (1) the peaked nature of the G vs. size relationship makes application of ANCOVA problematical and (2) the great variability in G (Fig. 1) combined with the necessarily low number of degrees of freedom result in a relatively low-powered test (Cohen, 1977). Maximum and minimum measured values for gross production efficiencies [(GPE) (mm’ growth. (mm’ sediment egested) ‘)I of small (I 0.5 mm’) worms were much greater than those of larger individuals and show a curvilinear decline with increasing BY (Fig. 8a). Animals less than z 1 mm3 (w 250 pg DW) show both the highest and lowest GPE values (Fig. 8a). After worms reached BY values of greater than z 1 mm3, GPE remained fairly constant at 2-3% (Fig. 8a). Pooled mean GPE was 8% = 4.771, N = 76). A predicted GPE curve calculated from G vs. BV (this study) and egestion rate vs. BT/(Forbes, 1989a; Forbes & Lopez, 1989) predicts greater GPE values in smaller (< 1 mm’) worms (Fig. 8a). The variability of measured GPE values about the predicted curve was much greater for the smaller worms (< 1 mm3) (Fig. 8b). These “residual” production efficiencies were skewed slightly toward the negative (SD

values for the smallest

animals.

DISCUSSION GROWTH

RATE

AND

BODY

SIZE

IN CAPITELLA

SP. 1

Tenore & Chesney (1985) and Marsh et al. (1989) have reported mass-specific maximum growth rates in Cupitellu sp. 1 ranging from 14.7 to 21 y0 . d- ’ on highnitrogen diets. These growth rates were size-dependent with greater G values in smaller worms. The results of the present study also show a size-dependent decrease in G, but only after animals reach sizes > 3 mm3 BV. Worms smaller than z 0.5 mm3 BY appear to grow at greater rates with increasing size (Fig. 1). The ontogenetic correlation of the peak in growth rates with a slightly narrower peak in V,, suggests a possible functional relationship between G and V,, up to body volumes

GROWTH

AND EGESTION

IN CAPITELLA

217

of z 2-3 mm3 (Figs. 1,2). These coincident peaks are consistent with previous results using an allometric approach in which speci~c-egestion rate in Capi~~~~a sp. 1 increased as a function of body size until animals reached volumes of 2.7 mm3 and then declined with further growth (Forbes, 1989a; Forbes & Lopez, 1989). Previous estimates of the scaling of particulate gut turnover time (h . gut ’ ) for this species suggest a minimum of M45 min at BV values between 1 and 1.5 mm3 (Forbes, 1989b). An observed minimum in gut turnover time corresponding to the plateau in V,, vs. BV would be expected if gut fullness does not change with size. That is, the relationships between GPT and V,, will be mirror images of each other if gut packing remains constant. Thus smaller worms (< 1.5 mm3 BP) appear to be increasing V,, at the expense of gut residence time. The associated growth-rate peak for worms of this size strongly suggests the net rate of energy gain may also be maximised at these intermediate worm sizes. The peaked nature of the G vs. body size relationship is also in contrast to standard growth models which universally predict a decreasing specific growth rate as a function of size (see Kaufmann, 1981). The present data suggest lower special-growth rates in both the smallest and largest animals. Assuming a continuously full gut and given the inverse relationship between gut turnover time (time sgut _ ’ ) and egestion rate (guts. time- ‘) and that it is advantageous for juvenile Cupitellu to minimize developmental time, these data suggest two possibilities. The first is that the balance between egestion rate (mm3 * h- ‘) and absorption rate was not optimized for smaller worms (co.5 mm3, Fig. 1). By not optimized we mean that simple changes in egestion rate or gut fullness could have increased absorption and/or growth rates. Alternatively, if the ratio of egestion rate to absorption rate was optimized to maximize growth rates, this suggests that there are fundamental constraints placed on the growth of small worms that cannot be compensated for by simple adjustments in egestion rate. Additional constraints that do not apply to juvenile worms after they reach sizes of ~0.5 mm’. We suggest that a promising approach to the resolution of these important problems would be the use of recently developed methods for the measurement of time-dependent absorption (K,) and egestion rates in very small juveniles (Kofoed et al., 1989). These techniques allow quanti~cation of the relationship between food digestibility and turnover time. The mean growth rate of 15% . d- ’ observed in this study is within the range of maxima found by Tenore and Chesney (1985). Thus the food mixture used in the present experiments appears to be adequate for the prevention of growth limitation due to a lack of assimilable nitrogen. This suggests that growth rates of E IS-20% . d - ’ are close to the maximum sustainable rates of individual worms. In an earlier study of the growth of juvenile C~p~~e~Z~ sp. 1, Marsh et al. (1989) found that small animals (l-60 lg DW) fed Gerber’s mixed cereal showed a size-dependent plateau of G at body dry weights of 40-50 ,ug for a wide range of R : B ratios. The results of the present study also suggest that small juvenile worms may exhibit relatively low growth rates. However the estimated plateau region in the present study began at slightly larger worm sizes and was much broader, extending from 0.5 to 3 mm3 BV (Fig. 1)

T.L. FORBES

218

AND G.R. LOPEZ

(z 120-720 pg DW; assuming a worm density = 1.07 mg. mm3 and DW: WW = 0.225; Cammen, 1985). The smallest worms show a much wider range of GPE with production efficiency values ranging from - 10 to 500/, (Fig. 8a). The primary sexual characters (i.e. copulatory setae, developing ovaries) in Cupiteh sp. 1 begin to appear at different body sizes in male as opposed to female worms, but do not appear at body sizes less than z 1 mm3 (TF, pers. obs.). Males begin to develop copulatory setae at a mean body volume of 1.3 mm3 (N = 3, SD = 0.46) and females of somewhat larger sizes contain developing eggs (2.9 mm3 SV, N = 4, SD = 0.95). All animals less than z 1 mm3 are sexually immature. Thus it is the sexually immature individuals that show the greatest variability of growth with respect to sediment-processing rate (Fig. 8a). THE DECOUPLING

OF GROWTH

AND

SEDIMENT-PROCESSING

RATE

One of the most interesting results of these experiments is the finding that growth is decoupled from the total volume of sediment processed during the growth measurement period. Given the positive relationship between G and V,,, this lack of correlation is probably due to the relatively large changes in egestion rate that are related to body size changes during growth. Because pellet bulk density is constant with respect to worm size, growth is also independent of the total mass of sediment egested (TF, unpubl. data). This result is not due to a time lag between total sediment processed and subsequent growth. Cross-correlation analysis revealed no correlation between growth and sediment processed (total sediment egested over the growth period (mm’)) for time lags of between 2 and 28 d. The lack of a relationship between total sediment egested and G implies that the cost of ingesting and processing sediment is relatively insignificant. Similarly, in recent work with ~~u~e~~c~~~pac$ca Taghon (1988) found no relationship between growth rate and egestion rate. ENVIRONMENTAL

“GRAIN”

AND

ABSOLUTE

BODY

SIZE

It is unclear whether the size-dependence of GPE is due to direct differences in the quality of the food consumed or to other factors. This increased variability in the transfer efficiency of food into tissue suggests that smaller worms have a greater sensitivity of response to environmental variables. For example, the variability of GPE in small worms may be related to absolute body size differences relative to the patch size and distributional scale of the food resource. This hypothesis views the growth of small worms as a response to real variation in the available energy content of food consumed over time. The experimental food consisted of ground Gerber’s mixed cereal and natural silt-clay sediment mixed in a controlled ratio (1 cereal: 3 sediment, V: V). Related growth experiments revealed that after having been frozen, the sediment alone produced little or no growth (TF, unpubl. data). Because of absolute size differences, the smaller worms may have experienced a much greater heterogeneity of the food mixture. If worms were unable to discriminate on the basis of the nutritional content of the available

GROWTH

AND EGESTIONIN

CAPI7XLA

219

food, one would expect a much greater variability in the nutritional content and digestibility of food consumed by the smallest animals. That is, the perceived environmental “gram” for these small microphages may be a function of absolute body size. The spatial distribution and abundance of available food may be absolute with respect to the size of a growing deposit-feeder, thus making the smallest individuals relatively more “macrophagous”. Clarification of these relationships is clearly important to an understanding of deposit feeder population dynamics. A combination of laboratory and field experiments utilizing mixtures of radiolabeled artificial and natural foods would be an appropriate first step in determining how changes in absolute size relate to a microphage’s ability to ingest and absorb foods. Alternatively, it may be that factors other than short-term food intake are primarily responsible for the growth response of the smallest worms. Small Cupitella sp. 1 are known to have a greater response to temperature both in terms of energy intake and expenditure (Cammen, 1985; Forbes & Lopez, 1987). Small scale changes in such environmental variables as temperature and food level would therefore be expected to have an increased effect on the smaller animals. ACKNOWLEDGEMENTS

We thank V. Brock, A. Carlson, R. Cerrato, M. Depledge, V. Forbes, L. Kofoed, R. Malouf, and G. Taghon whose critical reviews have greatly improved this manuscript. This research was supported by NSF grant OCE-85-01140 to G. R. Lopez. REFERENCES Brown, R. L., J. Durbin & J. M. Evans, 1975. Techniques for testing the constancy ofregression relationships over time. J. R. Stat. Sot., Vol. 37 B, pp. 149-163. Calow, P. & C. R. Townsend, 1981. Energetics, ecology and evolution. In, Physiologica/ ecology: an evolutionary approach to resource use, edited by C. R. Townsend and P. Calow, Sinauer Associates, Sunderland, Massachusetts. Cammen, L. M., 1985. Metabolic loss of organic carbon by the polychaete ~ap~fe~~acapitata (Fabricius) estimated from initial weight decrease during starvation, oxygen uptake, and release of 14C by uniformly labeled animals. Mar. Ecol. Prog. Ser., Vol. 21, pp. 163-167. Chesney, Jr., E.J., 1985. Succession in soft-bottom benthic environments: are pioneering species really outcompeted? In, 19th European Marine Biological Symposium, edited by P. E. Gibbs, Cambridge University Press, Cambridge. Chesney, Jr., E. J. & K. R. Tenore, 1985. Oscillations of laboratory populations of the polychaete Cap~~e~~a capizata (Type I): their cause and implications for natural populations. Mar. Ecul. Prog. Ser., Vol. 20, pp. 289-296. Cleveland, W. S., 1979. Robust locally weighted regression and smoothing scatterplots. J. Am. Srar. Assoc., Vol. 74, pp. 829-822. Cleveland, W. S. & R. McGill, 1984. The many faces of a scatterplot. J. Am. Scat. Assoc., Vol. 79, pp. 807-822. Cohen, J., 1977. Sta~isti~aipo~er a~za~~is~~ the ~ehaviara~sciences, Academic Press, New York, revised edition, 474 pp. Forbes, T. L., 1989a. The importance of size-dependent processes in the ecology of deposit-feeding benthos. In, Ecologic of marine depositfeeders edited by G. R. Lopez et al., Springer-Verlag, New York.

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AND G. R. LOPEZ

Forbes, T.L., 1989b. The importance of size-dependent physiological processes in the ecology of the deposit-feeding polychaete Capifella species I. Ph. D. diss., State University of New York, Stony Brook, New York, 180 pp. Forbes, T. L. & G. R. Lopez, 1989. Determination of critical periods in ontogenetic trajectories. Funct. Ecol., Vol. 3, pp. 625-632. Forbes, T.L. & G.R. Lopez, 1987. The allometry of deposit feeding in Capitella species I (Polychaeta: Capitellidae): the role of temperature and pellet weight in the control of egestion. Biol. BUN. (Woods Hole, Muss.), Vol. 172, pp. 187-201. Gremare, A., A.G. Marsh & K.R. Tenore, 1988. Short-term reproductive responses of Capitella sp. 1 (Annelida: Polychaeta) fed on different diets. J. Exp. Mar. Biol. Ecol., Vol. 123, pp. 147-162. Gremare, A., A. G. Marsh & K. R. Tenore, 1989a. Fecundity and energy partiotioning in Cupitella capitata type I (Annelida:Polychaeta). Mar. Biol., Vol. 100, pp. 365-371. Grtmare, A., A.G. Marsh & K.R. Tenore, 1989b. Secondary production and reproduction of Capitella cupitatu type 1 (Annelida:Polychaeta) during a population cycle. Mar. Ecol. Prog. Ser., Vol. 51, pp. 99-105. Kaufmann, K. W., 1981. Fitting and using growth curves. Oecologia (Berlin), Vol. 49, pp. 293-299. Kofoed, L. H., V. E. Forbes & G. R. Lopez, 1989. Time-dependent absorption in deposit feeders. In, Ecology of marine deposit feeders, edited by G. R. Lopez et al., Springer-Verlag, New York. Lopez, G. R. & J. S. Levinton, 1987. Ecology of deposit-feeding animals in marine sediments. Q, Rev. Biol., Vol. 62, pp. 235-260. Marsh, A.G., A. Gremare & K.R. Tenore, 1989. Effect of food type and ration on growth of juvenile Capiteila sp. I (Annelida: Polychaeta): macro- and micronutrients. Mar. Biol., Vol. 102, pp. 519-527. Nickerson, D.M., D.E. Facey & G.D. Grossman, 1989. Estimating physiological thresholds with continuous two-phase regression. Physiol. Zool., Vol. 62, pp. 866-887. Protter, M. H. & C. B. Morrey Jr., 1964. Volumes of solids of revolution. In, Modern mathematical analysis, Addison-Wesley, Reading, Massachusetts. Sibly, R. M. & P. Calow, 1986. Physiologicalecology of animals: an evolutionary approach. Blackwell Scientific Publications, London. Taghon, G.L., 1988. The benefits and costs of deposit feeding in the polychaete Aburenicolapacifica. Limnol Oceanogv., Vol. 33, pp. 1166-1175. Tenore, K. R., 1981. Organic nitrogen and the caloric content ofdetritus. I. Utilization by the deposit-feeding polychaete Capiteliu cupitatu. Estuarine Coastal ShelfSci., Vol. 12, pp. 39-47. Tenore, K. R., 1983. Organic nitrogen and caloric content ofdetritus.,3. Effect on growth ofa deposit-feeding polychaete, Cupitellu cupitatu. Estuurine Coastal ShelfSci., Vol. 17, pp. 733-742. Tenore, K. R. & E. J. Chesney, 1985. The effects of interaction of food supply and population density on the bioenergetics of the opportunistic polychaete, Capitella capituta (Type I). Limnol. Oceanogr., Vol. 30, pp. 1188-l 195. Tenore, K. R., L. Cammen, S. E. Findlay & N. Phillips, 1982. Perspectives in factors controlling detritus mineralization depends on detritus source. J. Mar. Res., Vol. 40, pp. 473-490.