The use of growth and ingestion rates of Capitella sp. I as the bioassay approaches to determine the sediment quality of coastal wetlands of Taiwan

Journal of Experimental Marine Biology and Ecology 297 (2003) 179 – 202 www.elsevier.com/locate/jembe

The use of growth and ingestion rates of Capitella sp. I as the bioassay approaches to determine the sediment quality of coastal wetlands of Taiwan Shin-I Hu a, Ching-Yi Horng b, I-Jiunn Cheng a,* b

a Institute of Marine Biology, National Taiwan Ocean University, Keelung 202-24, Taiwan, ROC Department of Occupational Safety and Health, Chang Jung Christian University, Tainan 717, Taiwan, ROC

Received 21 March 2003; received in revised form 9 May 2003; accepted 30 July 2003

Abstract Food is a limiting factor for the deposit feeders. The availability of sediment nutrients thus has a tight relationship with the growth, survival and development of the animal. There are two purposes of this study: (1) to determine if the ingestion and growth rates can be used as a bioassay approach to assess the sediment nutrients; and (2) use the combination of bioassay approaches and chemical analyses to determine which chemical parameter is the better predicator of the sediment nutrients to the animals. In the preliminary study, the optimal growth length and average ingestion rate of Capitella sp. I were obtained from the laboratory. The standardized relationships of the growth and ingestion rates in response to different nutrients were prepared. Then, the sediments collected from different coastal wetlands in Western Taiwan were used in the feeding, growth experiments and chemical analyses. The comparisons were made between the field and laboratory experiments to determine the sediment nutrients in the wetland of Taiwan. In the growth rate standardized relationship, Capitella sp. I increased its growth rate with the total organic nitrogen (TON) concentration between 0 to 2.8 mgN
g sediment 1, total organic carbon (TOC) concentration between 0 and 22.4 mgC
g sediment 1, and enzymatically hydrolyzable amino acid (EHAA) concentration between 0 and 4.48 mg protein
g sediment 1. After the nutrient concentrations exceed these values, the growth rates decreased gradually. In the ingestion rate standardized relationship, the animal increased its ingestion rate with the total organic nitrogen (TON) concentration between 0 and 2 mgN
g sediment 1, total organic carbon (TOC) concentration between 0 and 14.1 mgC
g sediment 1, and EHAA concentration between 0 and 3.2 mg protein
g sediment 1. After the nutrient concentrations exceed these values, the ingestion rates also decreased. To determine which nutrient parameter is the best predictor for the sediment nutrient in the field, we first analyzed whether the data obtained from the laboratory fell within 99% confidence interval of the regression

* Corresponding author. Tel.: +886-2-24622192x5303; fax: +886-2-24628974. E-mail address: [email protected] (I.-J. Cheng). 0022-0981/$ - see front matter D 2003 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2003.07.009

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obtained from the field data. Then, to determine which parameter had the shortest perpendicular distance between the field and the laboratory regression curves. Both the growth and ingestion rates comparisons showed that the EHAA is the best candidate of the sediment nutrient of deposit feeders in the field. The results of this study proved tentatively that the growth and ingestion rates of Capitella sp. I can be used as the bioassay approaches to estimate the sediment nutrients. The combination of the bioassay approaches and the relevant chemical analyses allows us to determine the bioavailability fraction of sediment to the deposit feeders. D 2003 Elsevier B.V. All rights reserved. Keywords: Bioassay approach; EHAA concentration; Growth rate; Ingestion rate; Sediment nutrients

1. Introduction Deposit feeders obtain their nutrients from the sediment and are the important secondary producers in wetland ecosystems. They play a central role in transferring both energy and material from primary producers and detritus to organisms, such as fishes and birds, in the higher trophic levels (Wurzian, 1984; Mitsch, 1993). However, the sediment is mainly composed of inorganic matter, and most detritus is non-labile in nature (Bayne and Newell, 1983; Hughes, 1970; Lopez and Levinton, 1987; Mayer, 1987). The deposit feeders are generally food-limited (Lopez and Levinton, 1987; Mayer 1989). The availability of nutrients on sediment particles can then influence the growth and survivorship of these animals (Marsh et al., 1989; Qian, 1994; Qian and Chia, 1992; Tenore, 1983; Tenore and Chesney, 1985), and, thus, the organisms in the higher trophic levels. In order to obtain enough food, some deposit feeders behave selective feeding (Lopez and Cheng, 1982; Levinton et al., 1984; Taghon and Jumars, 1984). They also change their ingestion rates, especially when food availability is limited, to maintain the homeostasis of metabolism (Bayne and Newell, 1983; Calow, 1975; Phillips, 1984; Taghon, 1981). Animals may increase their ingestion rates with the increase of food concentrations in order to obtain more nutrients (Taghon, 1981; Tenore, 1977; 1981). They may also decrease their ingestion rates with the increase of food concentrations in order to increase the absorption efficiency of ingested nutrients (Cammen, 1980). Forbes et al. (1994) found that the ingestion rate of polychaete Capitella sp. I increase with the sediment protein concentration. Hrong (1998), however, found that the ingestion rate of this animal could decrease with the addition of cereal (Gerber’s Mixed Cereal), as the protein supplement, to the sediment. The sediment nutrients can influence the feeding behavior of deposit feeders. This, in turn, affects the growth and reproduction, thus the fitness of animal (Qian and Chia, 1992; Levin et al., 1986; Marsh et al., 1989; Tenore, 1983; Tenore and Chesney, 1985). Among all general chemical parameter tested, nitrogen-containing material appears to represent the sediment nutrition (Hrong, 1998; Marsh et al., 1989; Tenore, 1977). Hrong (1998), however, also found that the fungal protease hydrolyzable peptides, named enzymatically hydrolyzable amino acid (EHAA) by Mayer et al. (1995), of sediment was a better growth indicator for Capitella sp. I, compared with sedimentary carbon and nitrogen. EHAA is

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essentially a biomimic approach that measures both small and large peptides, which could be hydrolyzed by protease. Linton (1999) further evidenced that the size of Capitella sp. I was larger when fed on sediments with higher EHAA concentrations. The sediment nutritional values to deposit feeders can be estimated by two methods; the chemical analyses and bioassay approaches. The chemical indicators frequently used include TOM, TOC, TON, chlorophyll (Cheng et al., 1993; Page et al., 1992), labile protein (Mayer et al., 1986), and EHAA (Mayer et al., 1995) concentrations of sediment. These sedimentary chemical parameters, however, may not represent the total available fraction to the animals. The deviation may even become larger when the approach is applied to field sediments with heterogeneous nature. Particle size distribution (e.g. Hrong, 1998) and pollutant contents (e.g. Chen et al., 2002) may serve as confounding factors to restrain the prediction of these chemical parameters. Because the food availability can influence the nutrient uptake and absorption, the feeding and growth responses of deposit feeders can also be used as the bioassay approaches to determine the sediment nutritional values (Cheng et al., 1993). The ingestion rate can represent the response of individual animals to the change of the food quality. The growth rate of immature animals, on the other hand, reflects the amount of energy assimilated after food ingested and absorbed. That is, more growth in a similar feeding rate simply implies that the sediment they fed on contained more labile nutrients. Thus, the combination of both ingestion and growth rates can estimate the bioavailability of sediment to the animals (Fang, 2000; Hargrave, 1970). The chemical analyses cannot be used as the sole indicators of the sediment nutrient. The bioassay method, on the other hand, is not able to determine which sediment nutrient act as the limiting factor to the animals. The combination of these two methods can determine not only the limiting nutrient to the animals, but also its availability in the field. Capitella sp. I is an opportunistic deposit feeder, which commonly inhabits in muddy estuarine sediments. The size of the cultured adult worms ranges from 20 to 40 mm, and the wet weight ranges from 3 to 12 mg. It has the life history characters of fast growth and short generation time (35 – 45 days at 20 jC). Capitella sp. I resides in one place for several months to a year, and achieves an explosive population growth in response to a sudden organic loads or disturbance of the environment. Capitella sp. I, thus, is commonly used as a pollution indicator (Giangrande and Montanaro, 1997; Grassle and Grassle, 1974, 1976). There is a close relationship between the growth of Capitella sp. I and nutrient content of sediment. The feeding behavior of this animal was also found to change with food supply (Forbes and Lopez, 1990; Marsh et al., 1989; Tenore, 1977). Thus, the purposes of this study were to test (1) whether the ingestion and growth rates of the deposit-feeding polychaete Capitella sp. I can be used as a bioassay to estimate the sediment bioavailability, and (2) which chemical parameter in sediment can act as the best predictor of the sediment nutritional value, i.e. the change of its concentration can influence the growth and ingestion rates of the animal more than the other materials do.

2. Materials and methods Culture of Capitella sp. I (Grassle and Grassle, 1976) was obtained from Dr. J.P. Grassle’s laboratory at Rutgers University (New Jersey, USA), and raised in our laboratory

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for at least two generations prior to the experiment. The animals were kept in the seawater table with constant water temperature (20 jC) and salinity (30x ). The animals used for the experiments were the 3-week-old juveniles. Their width of the fifth setiger was at a range of 0.5– 0.7 mm. The experiments were separated into two parts. In the first part, food-amended sediments were used to determine the relationship between the known food concentrations and the responses of Capitella sp. I, in terms of growth rate and ingestion rate. These relationships were designated as the ‘‘standardized relationship’’. In the second part, similar bioassay experiments and chemical analyses, but with sediments from various wetland mudflats in the western Taiwan, were conducted. Then, the comparisons were made between the two to (1) examine whether the Capitella bioassay was sensitive enough to represent the food quality of different field sediments, (2) determine which chemical parameter was the better indicator for the sedimentary nutrition, and (3) assess the nutritional values of the wetland mudflats in Taiwan. 2.1. Determine the ‘‘standardized relationship’’ in the laboratory 2.1.1. Growth rate experiment 2.1.1.1. Preliminary experiment. The purpose of the preliminary experiment was to determine the length of day that the juvenile worms needed to reach the maximum body size. The width of the fifth setiger of five animals were measured under a dissecting microscope (Ziess, Stemi 2000-C model), and placed in a glass finger bowl (5 cm in diameter), bottom covered with 10 g 0.105 mm-sieved sediment collected from Chuwei Mangrove Forest (Cheng, 1995; Cheng and Chang, 1999). Six replicates were prepared and cultured in a seawater table. The experiment was conducted in the alternation of light and dark periods in a 12-h cycle. The width of fifth setiger of individuals was measured every 3 days. No new sediment was added to the finger bowl during the experiment. The experiment was terminated after a confirmed decrease in worms’ width, i.e. the mean widths were lower than the previous measurement. The results showed that the animals reached the maximum body size in 6 days of culture (Fig. 1). Thus, the duration of the following growth experiments in this study were set to 6 days. 2.1.1.2. The ‘‘standardized relationship’’ experiment. First, the TOC, TON and EHAA of the Chuwei Mangrove Forest sediment were measured (the measurements of TOC, TON, and EHAA were detailed in later section). Then, various amounts of the fish food powder were added to the Chuwei sediment as the nutrient supplements. The TOC, TON, and EHAA of the fish food were also measured prior to the experiment. Because there existed a positive relationship between the growth rate of Capitella sp. I and the nitrogenous content of the sediment (Hrong, 1998), and because we did not establish the EHAA measurement until 1999, TON was used to represent the amount of nutrient in the ‘‘standardized relationship’’ experiment, and expressed as the mgN g sediment 1. Fourteen sediments of various organic concentrations were prepared by mixing the mangrove sediment with various amounts of fish food powder as listed in Table 1. For treatments that the assigned nitrogen value lower than the nitrogen content of the

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Fig. 1. The preliminary growth experiment of Capitella sp. I used to determine the maximum culture period for the animals fed on the same batch of sediment. Six replicates were use in this experiment.

mangrove sediment, ashed sediment was added. The range of nitrogen concentrations selected for this experiment covered the range used in the published data of the sediments from Taiwan (the lower end of the listed concentrations) (Chen and Lin, 1996; Cheng and Chang, 1999; Chen, 2001), and the U.S. (the higher end of the listed concentrations) (Linton, 1999). The protocol of culture preparation has been described in the previous section. Three replicates of each group were prepared. The experiment lasted for 6 days and the width of fifth setiger of each worm was measured prior and after the experiment. The growth rate was calculated as follows: Growth rate ðmm day1 Þ ¼ ðfinal width  initial widthÞ=6 ðdaysÞ 2.1.2. Ingestion rate experiment Hargrave (1970) suggested that the quantity of sediment ingested by worm-like deposit feeder is similar to the quantity of sediment egested. Thus, the egestion rate of worm is comparable to its ingestion rate. Table 1 The total organic nitrogen (TON) contents of sediment prepared for the standardized relationship experiment of both ingestion and growth rates of Capitella sp. I in the laboratory Treatment

1

2

13

14

TON concentration (mgN g sediment 1)

0

0.05 0.1 0.15 0.2 0.8 1.4 2.0 2.8 3.6 4.4 5.4 6.4

7.4

Ashed sediment (g) (0 mgN
g 1) 10 9.4 Sediment (g) (0.8 mgN
g 1) 0 0.6 Fish food (mg) (62.3 mgN
g 1) 0 0

3

4

8.7 8.1 1.3 1.9 0 0

5

6

7

8

9

10

11

12

7.5 0 0 0 0 0 0 0 0 0 2.5 10 10 10 10 10 10 10 10 10 0 0 99 199 336 477 622 808 1002 1202

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2.1.2.1. Preliminary experiment. The purposes of this experiment were to determine whether we can collect enough feces in 3 days and to assess the variability among individual animals. The 3 days was set to offset the abnormal feeding behavior due to the disturbance caused by the experimental preparation. Twenty-five animals were placed individually in glass finger bowls, bottom covered with 2 g 0.105-mm sieved Chuwei Mangrove Forest sediment. They were cultured in a seawater table for 3 days with 12h cycles between light and dark conditions. The animals were then removed. Because the feces of Capitella sp. I are football shape with a minimum width about 0.2 mm, the remaining sediment was sieved through a 0.105-mm sieve. The fecal pellets were collected by a pipette under a dissecting microscope, placed on a pre-weighted filter (1.2 Am, 2.4 cm in diameter), and dried in an oven (100 jC) for 24 h. The dried feces were weighed, and the ingestion rate was calculated as follows: Ingestion rate ðmg h1 Þ ¼ dried feces weight=feeding time ð72 hÞ The results showed that the average ingestion rate is 0.12 F 0.09 mg h 1. 2.1.2.2. The ‘‘standardized relationship’’ experiment. Based on Table 1, 14 groups of 2 g sediment varying in nutrient contents were prepared. For each treatment, one animal was cultured in each glass finger bowl and five replicates were prepared. The experimental protocol has been described in the previous section. 2.2. Field sediment collections, feeding experiments and chemical analyses 2.2.1. Field sediment collections Nine wetland mudflats from the west coast of Taiwan were chosen (Fig. 2). Because they are the only existing mangrove forests in Taiwan, the results of this study may represent the relative availability of sedimentary nutrient among the precious mangrove habitats of Taiwan. The sediments were collected between November and December of 2000. In each mudflat, three sampling spots with 10 m apart were chosen at random. In each site, top 5 – 10 cm depth sediment was collected. They were then mixed completely to reduce the spatial variation. The sediment samples were sieved in the field through a 1-mm mesh sieve to remove larger particles and macrofauna. They were then stored in a plastic cooler and transported back to the laboratory immediately. In the laboratory, the sediments were sieved again through a 0.105-mm sieve in order to obtain the sediment with the same size range as the standardized experiments. In order to keep the sediment quality, samples were stored in a freezer (  20 jC) prior to the experiment. 2.2.2. Feeding experiment 2.2.2.1. Growth rate experiment. A total of 225 animals were assigned randomly to the nine field sediment treatments. For each treatment, five animals were cultured in each dish and five replicates were prepared. The experimental protocol is the same as described in the previous section.

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Fig. 2. The sites of mudflats in the western Taiwan where the sediments were collected for the feeding experiments.

2.2.2.2. Ingestion rate experiment. Ninety animals were assigned randomly to the nine field sediment treatments. For each treatment, one animal was cultured in each dish and 10 replicates were prepared. The experimental protocol is the same as described in the previous section. 2.2.3. Sediment chemical analyses For chemical analyses, the total organic matter (TOM), total organic carbon (TOC), total organic nitrogen (TON), and enzymatically hydrolysable amino acid (EHAA) of the

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sediment were determined. The TOM was determined by an ash-free-dry-weight method (AFDW). The samples were dried in an oven (100 jC) for 6 h, and then ashed in a muffle furnace for 12 h (500 jC). Few drops of distilled water were added to the ashed sediment to regain the crystal water. The TOM was determined by the following equation: TOMð%Þ ¼ ½1  ðashed weight=dried weightÞ  100% Organic carbon and nitrogen contents were analyzed by a CHN-Elemental Analyzer (Perkin-Elmer Model 2400 Series II). Freeze-dried samples were acidified with concentrated HCl vapor overnight to remove inorganic carbonate before analysis. The unit is expressed as % (w/w). Sediment protein concentration was determined using the EHAA (enzymatically hydrolyzable amino acid) technique of Mayer et al. (1995), which is a biomimetic assay of digestible protein based on direct incubation of sediments with a fungal proteolytic enzyme. The unit is expressed as mg EHAA g sediment 1. 2.2.4. Statistical analysis The relationships between the physiological responses of worms and food concentrations were determined by regression correlation analyses (Sokal and Rohlf, 1982). Coefficient of determination (r2) and significant value ( p) of the regression models were calculated through ANOVA procedure for comparison. Two sets of data (i.e. laboratory and field sediments) were compared to determine whether the ‘‘standardized relationship’’ of both ingestion and growth rates obtained from the laboratory would apply to that in the field. Because the ingestion and growth rate data obtained from the experiment with field sediments were more variable than the experiment with laboratory sediments, the ‘‘standardized relationship’’ was compared with 99% confidence interval of the regression obtained from the experiment with field sediments (Sokal and Rohlf, 1982). Then, Student’s t-tests were performed on the slopes and elevations between these two regression lines to determine whether these two data sets belong to the same population (i.e. parallel lines) or belong to the different populations (i.e. non-parallel lines) (Zar, 1999). Once non-significant difference of slopes and elevations of the two regression lines were concluded, the average perpendicular distances from every mean value of the field sediment to the standardized regression line were calculated to determine which chemical indicator, among the TOC, TON, and EHAA, provided a better predictability for the nutritional value of the field sediment. That is, the closer standardized regression line to the field sediment experiments implied a better predictability of the chemical indicator applicable in the field sediments.

3. Results 3.1. Standardized relationship of both growth and ingestion rates In the standardized growth and ingestion experiments, results showed consistently that the growth and ingestion rates increased with the increase of food concentration to a certain intermediate value, then decreased with further increase of food concentration (Figs. 3 and 4). To describe the bimodal relationships between food concentrations and

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Fig. 3. Standardized growth rate experiment based on the food-amended sediments. (a) The nutrient concentration based on TON values, (b) the nutrient concentration based on TOC values, and (c) the nutrient concentration based on EHAA values. Error bars indicate S.D.

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Fig. 4. Standardized ingestion rate experiment based on the food-amended sediments. (a) The nutrient concentration based on TON values, (b) the nutrient concentration based on TOC values, and (c) the nutrient concentration based on EHAA values. Error bars indicated S.D.

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physiological responses of worms, we conducted curve fitting with both polynomial regression and two-step linear regression. In the two-step linear regression, the data were divided into two groups by the apparent turning point of the curve. Each group was analyzed separately with a linear regression analysis. The two-step linear regression lines were chosen to describe the relationship between sedimentary food concentrations and physiological responses of worms due to its higher yields of r2 values. In addition, the trends can be explained more logically by separate the data into two groups in terms of animal physiology. 3.1.1. Growth rate experiment The relationships between the growth rate and sediment TON, TOC, and EHAA are shown in Fig. 3a, b, and c, respectively. Treatment 13, of which the designated nitrogen content was 6.4 mgN g sediment 1, was omitted from regression analyzes due to its odd elevation of growth responses. The growth rate increased with increasing TON from 0 to 2.8 mgN g sediment 1 ( y =  0.0058 + 0.0319x, r2 = 0.99, p < 0.01, n = 9), then decreased gradually after the value exceeds 2.8 mgN g sediment 1 ( y = 0.0958 – 0.0061x, r2 = 0.94, p < 0.01, n = 5). The growth rate increased with increasing TOC from 0 to 22.4 mgC g sediment 1 ( y =  0.0058 + 0.004x, r2 = 0.99, p < 0.01, n = 9), then decreased gradually after the value exceeds 22.4 mgC g sediment 1 ( y = 0.0958 – 0.0008x, r2 = 0.94, p < 0.01, n = 5). The growth rate increased with increasing EHAA from 0 to 4.48 mg EHAA g sediment 1 ( y =  0.0058 + 0.0199x, r2 = 0.99, p < 0.01, n = 9), then decreased gradually after the value exceeds 4.48 mg EHAA g sediment 1 ( y = 0.0958 –0.0038x, r2 = 0.94, p < 0.01, n = 5). In the low food concentration (such as TON from 0 to 0.15 mgN g sediment 1), animals either experienced negative growth or death. However, a few animals were found mature and containing eggs. These phenomena will be discussed in the Discussion section. 3.1.2. Ingestion rate experiment The relationship between the ingestion rate and sediment TON is shown in Fig. 4a. The ingestion rate increased with increasing TON from 0 to 2 mgN g sediment 1 ( y = 0.0667 + 0.2148x, r2 = 0.56, p < 0.05, n = 8), then decreased after the value exceeds 2 mgN g sediment 1 ( y = 0.5232– 0.0514x, r2 = 0.84, p < 0.01, n = 7). The relationship between the ingestion rate and sediment TOC is shown in Fig. 4b. The ingestion rate increased with increasing TOC from 0 to 14.1 mgC g sediment 1 ( y = 0.0667 + 0.0268x, r2 = 0.56, p < 0.05, n = 8), then decreased after the value exceeds 14.1 mgC g sediment 1 ( y = 0.5232 –0.0064x, r2 = 0.84, p < 0.01, n = 7). The relationship between the ingestion rate and sediment EHAA is shown in Fig. 4c. The ingestion rate increased with increasing EHAA from 0 to 3.2 mg EHAA g sediment 1 ( y = 0.0667 + 0.1342x, r2 = 0.56, p < 0.05, n = 8), then decreased after the value exceeds 3.2 mg EHAA g sediment 1 ( y = 0.5232 – 0.0322x, r2 = 0.84, p < 0.01, n = 7). 3.2. Sediment chemistry TOM, TOC, TON, and EHAA contents of the sediments used for the standardized relationship experiments and from various field sites are shown in Table 2. For TOM, the

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Table 2 TOM, TOC, TON and EHAA of the sediment used for the standardized relationship experiment from various mudflats in Taiwan Sediment used for/from Standardized relationship experiment Fish food Chu-wei Ba-li Hon-mau Shan-san Wen-to-je Kau-ma Haw-mei-laiu North gate Sie-tau

TOM 9.7 F 0.96 (8) – 10.2 F 1.59 3.4 F 0.73 5.5 F 0.21 3.0 F 0.38 5.1 F 0.14 1.7 F 0.28 7.3 F 0.41 3.5 F 0.51 3.5 F 0.26

(8) (8) (8) (8) (8) (8) (8) (8) (8)

TOC (mg G 1)

TON (mg G 1)

EHAA (mg G 1)

6.0 F 2 (5)

0.8 F 0.3 (5)

1.0 F 0.1 (12)

410 F 2 (5) 9.2 F 0.6 (5) 5.8 F 0.4 (5) 11 F 1.0 (5) 4.9 F 0.2 (5) 10 F 0.6 (5) 3.2 F 0.3 (5) 14 F 0.8 (5) 6.7 F 0.8 (5) 3.5 F 0.2 (5)

62 F 1 (5) 2.0 F 0.4 (5) 0.7 F 0.2 (5) 1.4 F 0.2 (5) 0.7 F 0.1 (5) 1.0 F 0.4 (5) 0.3 F 0.1 (5) 1.2 F 0.1 (5) 1.1 F 0.3 (5) 0.5 F 0.1 (5)

19 F 0.0 1.5 F 0.2 0.6 F 0.1 1.1 F 0.1 0.5 F 0.1 0.9 F 0.2 0.4 F 0.1 0.3 F 0.1 0.8 F 0.1 0.3 F 0.1

(12) (12) (12) (12) (12) (12) (12) (12) (12) (12)

The unit is w/w (%). The data are presented as: mean F standard deviation (number of replicates).

highest value (10.2%) of the field sediments collected was from Chu-wei mudflat, and the lowest was from Kau-ma mudflat (1.7%). For TOC, the highest value (14 mgC g sediment 1) of the field sediments collected was from Haw-mei-laiu mudflat and the lowest was from Kau-ma mudflat (3.2 mgC g sediment 1). For TON, the highest value (2.3 mgN g sediment 1) of the field sediments was collected from Chu-wei mudflat and the lowest was from Kau-ma mudflat (0.3 mgN g sediment 1). For EHAA, the highest value (1.5 mg EHAA g sediment 1) of the field sediments collected was from Chu-wei mudflat and the lowest were from Haw-mei-laiu and Sie-tau mudflats (0.3 mg EHAA g sediment 1). 3.3. Ingestion and growth rates obtained from the field sediments Results of the growth and ingestion rates of Capitella sp. I fed on the field sediments were listed in Table 3. The highest growth rate was 0.05 mm day 1 in Haw-mei-laiu mud. Negative growth rates were found when the animals fed on sediments from Ba-li, Shansan, and Wen-tou-je mudflats. The highest ingestion rate was 0.26 mg h 1 occurred in Table 3 The growth and ingestion rates of Capitella sp. I fed on various mudflat sediments of Taiwan Sites where sediments were collected

Growth rate (mm day 1)

Ingestion rate (mg h 1)

Chu-wei Ba-li Hon-mau Shan-san Wen-to-je Kau-ma Haw-mei-laiu North gate Sie-tau

0.04 F 0.03  0.04 F 0.03 0.00 F 0.01  0.02 F 0.02  0.02 F 0.01 0.01 F 0.03 0.05 F 0.07 0.02 F 0.03 0.02 F 0.03

0.23 F 0.1 (10) 0.20 F 0.13 (10) 0.07 F 0.04 (10) 0.08 F 0.07 (10) 0.12 F 0.04 (10) 0.08 F 0.04 (10) 0.26 F 0.13 (10) 0.13 F 0.09 (10) 0.17 F 0.11 (10)

(5) (5) (5) (5) (5) (5) (5) (5) (5)

The data are presented as: mean F standard deviation (number of replicates).

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Haw-mei-laiu mud, and the lowest was 0.047 mg h 1 in Hon-mau mud. Both ingestion and growth rates obtained from the field sediments were compared with the standardized relationships to determine which chemical parameter offers a better prediction for the food value of the field sediments. Fig. 5 shows the overlay of the field growth rate data on the standardized relationship curves. The field data were scattered wider than the standardized data. This is due to the

Fig. 5. The overlay of the field growth rate data (solid triangles) on the standardized relationship curve (solid diamonds). The dash lines represent 99% confidence interval of the regression obtained from the experiment with field experiments. Error bars indicate S.D. (a) TON, (b) TOC, and (c) EHAA concentration of field sediments.

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fact that the mingled sediments with designated amounts of fish food and ashed sediment tend to be more uniform and simpler, in term of nutrient composition, than the field sediments from various mudflats. The field sediments, however, are chemically heterogeneous in nature and may consist of various degrees of anthropogenic contamination, which may magnify the physiological responses of individual worms within sediment treatment. For this reason, comparison was made by fitting the ‘‘standardized relationship’’ data into 99% confidence interval of the regression obtained from the field sediment treatments. The results (Fig. 5) showed that the data of all three standardized curves (i.e. TOC, TON, and EHAA) fell within 99% confidence interval of the regression obtained from the field sediment treatments. This suggests that the food-amended sediments with lower concentrations for the standardized relationship experiment were in the similar population of the field sediments. Even though all three chemical indicators showed similar trends of worms’ growth rates for both the food-amended sediments and field sediments, we further test the statistical strength and determined which one showed the best prediction of the sedimentary nutritional value in the field. Comparisons were made on the slope and elevation of the regression lines obtained from the field sediments and the standardized ones (Zar, 1999). Results (Table 4) showed the regression lines of TON, TOC, and EHAA for the standardized experiment were paralleled to those obtained from the field sediment and had similar elevations. The average perpendicular distances from every mean value of the field sediment to the standardized regression line were 0.027, 0.023, and 0.025 for TON, TOC, and EHAA, respectively. One-way ANOVA showed the three average perpendicular distances are non-significant difference ( p>0.05). These results suggest that the three chemical indicators are all suitable to predict the sediment nutritional values. Fig. 6 shows the overlay of the field ingestion rate data on the standardized relationship curves. EHAA standardized data was the sole chemical indicator that fell within 99% Table 4 Comparisons of slope and elevation between regression line of standardized experiment and regression line of field sediment experiment TON Slope

TOC Elevation

Value Regression line of standardized experiment Growth rate 0.0319  0.0058 Ingestion rate 0.2148 0.0667 Regression line of field sediment experiment Growth rate 0.0236  0.0153 Ingestion rate 0.0515 0.0980

EHAA

Slope

Elevation

Slope

Elevation

0.0040 0.0268

 0.0058 0.0667

0.0199 0.1342

 0.0058 0.0667

0.0031 0.0084

 0.0150 0.0856

0.0018  0.0004

0.0067 0.1492

Stat t Growth rate Ingestion rate

0.529 –

1.822 –

0.418 –

1.658 –

0.890 1.222

0.088 0.282

p value Growth rate Ingestion rate

0.605 –

0.088 –

0.682 –

0.118 –

0.389 0.243

0.931 0.782

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Fig. 6. The overlay of the field ingestion rate data (solid triangles) on the standardized relationship curve (solid diamonds). The dash lines represent 99% confidence interval of the regression obtained from experiment with the field sediment. Error bars indicate S.D. (a) TON, (b) TOC, and (c) EHAA concentrations of the field sediments.

confidence interval of the field data. This suggested that the EHAA standardized regression line was the only one that has a similar trend as the field data. Comparisons of the slope and elevation between the ingestion rate regression lines obtained from the field sediments and the standardized ones for EHAA measurements showed that two lines were paralleled to each other and both had similar elevations (Table

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4). This also suggested that the EHAA concentration had a similar effect on the ingestion rate of Capitella sp. I both in the field experiment and in the standardized experiment.

4. Discussion Many studies showed that there were strong relationships between the sediment nutrient contents and the size of individual animal as well as the population density (Tenore, 1977; Levinton and Bianchi, 1981; Marsh et al., 1989; Hrong, 1998; Linton and Taghon, 2000). In this study, we tested how well the physiological response of the animal can be used as the bioassay approaches to predict the nutrition of sediment. The standardized relationships between worms’ physiological responses and sediment nutrient contents were first established by feeding experiments with food-amended sediments. Ingestion and growth rates were used as the physiological indicators. Then, another similar feeding experiment was conducted to test whether the standardized relationships held for worms in various field sediments. If the physiological responses between worms in food-amended sediments and those in field sediments are comparable, it might indicate the sediment nutrition in the field can be estimated quantitatively by the bioassay method we proposed.

5. Relationships between the sediment nutrient contents and the growth rate of Capitella sp. I in the food-amended sediments Fig. 3 showed that the growth rate of Capitella sp. I increased when the TON increased from 0 to 2.8 mgN g sediment 1, TOC increased from 0 to 22.4 mgC g sediment 1, and EHAA increased from 0 to 4.48 mg EHAA g sediment 1. These results were similar to the other studies (Tenore, 1983; Forbes and Lopez, 1990; Bridges et al., 1994; Gremare et al., 1988; Hrong, 1998; Linton and Taghon, 2000). The growth rate, however, decreased gradually after the food concentrations exceeded these optimum values. The possible reasons for the decrease in growth rate after organic concentration exceeds certain value are the bacterial activities increasing with the food availability, although the finite growth environment such as the finger bowl was used in this study. This may enhance the depletion of the dissolved oxygen in the culture. The growth condition of Capitella sp. I depends on both the food concentration and the available dissolved oxygen (Forbes and Lopez, 1990). The animals are likely to ingest and absorb foods more efficiently than to obtain the dissolved oxygen. Thus, the oxygen may be a limiting factor to the growth of Capitella sp. I (Forbes and Lopez, 1990). The other possibility is that in high food environment, the high microbial activities can result in the accumulation of metabolic products or toxic derivatives in the sediment. These materials can cause abnormal physiological response of the animals (Linton and Taghon, 2000). Thus, even in the high food environment animals may grow suboptimally. Animal grows negatively when the food intake less than the metabolic cost (Hughes, 1970; Townsend and Calow, 1981; Sibly and Calow, 1986). In the standardized relationship experiments, Capitella sp. I grew negatively in cultures with TON from 0 to 0.15 mgN g sediment 1, TOC from 0 to 1.2 mgC g sediment 1, and EHAA from 0 to

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0.24 mg EHAA g sediment 1. These results suggest that the minimum food concentration for Capitella sp. I to survive should be 0.15 mgN g sediment 1, 1.2 mgC g sediment 1, and 0.24 mg EHAA g sediment 1. The results of this study have proved that the growth rate did change with the food concentration. For example, in case of TON (Fig. 3a), one-way ANOVA showed that there was a significant difference between the growth rates in nine groups that fed with low food concentrations (i.e. between 0 and 2.8 mgN g sediment 1) and those in six groups that fed with high food concentrations (i.e. between 2.8 and 7.4 mgN g sediment 1) ( p < 0.05). Thus, we accept tentatively that the growth rate is sensitive to sediment nutrient contents and the standardized relationship is suitable to predict sediment nutrition in the field.

6. Relationships between the sediment nutrient contents and the ingestion rate of Capitella sp. I in the food-amended sediments Fig. 4 showed that the ingestion rate of Capitella sp. I increased when the TON increased from 0 to 2 mgN g sediment 1, TOC increased from 0 to 16 mgC g sediment 1, and EHAA increased from 0 to 3.2 mg EHAA g sediment 1. The ingestion rate of Capitella sp. I was reported to increase with increasing total organic nitrogen and protein concentrations in sediment (Forbes et al., 1994; Hrong, 1998). Linton (1999) found in the laboratory that the ingestion rate of this species increased with the protein concentration from 0.2 to 4.7 mg g sediment 1. She suggested that this result was consistent with the optimal foraging theory. In food-limited environment, deposit feeders change their ingestion rates to increase the food intake or energy absorption (Taghon, 1981; Calow, 1982; Phillips, 1984; Cammen, 1980; Dade et al., 1990). Worms’ ingestion rates in the lower end of nutrient content treatment in the present study were consistent with Linton’s (1999) argument. The ingestion rate, however, decreased after the nutrient concentrations exceed the optimum values. It is possible that in high food environment, animal increases its gut residence time to maintain the homeostasis of the energy absorption or decrease time for feeding (Cammen, 1980). Worms’ ingestion rates in the higher nutrient content treatment in the present study were consistent with Cammen’s (1980) compensatory hypothesis. Dade et al. (1990), however, suggested that the ingestion rate reached the maximum value at the intermediate food level, because the animal can obtain the maximum ingested energy with the highest ingestion rate at this food concentration. Our results indicated the worms’ responses over nutrient contents in the whole range of spectrum are consistent with his conclusion. Linton and Taghon (2000) found that the ingestion rate of Capitella sp. I increased with the protein concentration till 4.7 mg g sediment 1, then level off with further increase in food concentration in the laboratory. In our study, the ingestion rate of Capitella sp. I decreased after the protein concentration exceeds 4.48 mg g sediment 1. The laboratory conditions were almost similar between the two studies, except for the difference in the experimental design. In our study, only one worm was introduced to each dish instead of five worms in the Linton’s experiment. It is possible that the animal in our study experienced a better feeding environment (i.e. in terms of food supply and dissolved

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oxygen content) during the experiment. Thus, the response of the animal was more consistent with the Dade’s optimal foraging hypothesis (1990). That is, the ingestion rate reaches the maximum value at the intermediate food level. Suppose that if more than one worm were place into the same container, then the competition for food may occur. The more crowded environment in the Linton’s experiment might result in a less optimal feeding condition to the animals (Linton and Taghon, 2000). When the food concentration becomes too low to maintain the basic metabolic needs of the animals, they will either decrease their egestion rate substantially or stop feeding, and subsequent emigration or hibernation might occur (Sibly and Calow, 1986; Hymel and Plante, 2000). Similar phenomenon was observed in our study. In four treatments with low food concentrations (e.g. TON from 0 to 0.15 mgN g sediment 1), the ingestion rates were extremely low. This suggests that the worms were barely fed during the experiment. In addition, we observed some worms migrated out of the sediment, and climbed onto the wall up to the mouth of the finger bowl. Thus, in the case when the food availability is too low and the animals cannot find another food source, they will stop feeding to reduce the energy expenditure or emigrate to the other sediment environment. The results have also proved that the ingestion rate did respond to the change of food concentration. For example, in the case of TON (Fig. 4b), one-way ANOVA showed that there was a significant difference between the ingestion rates in eight groups of worms fed on low food concentrations (i.e. between 0 and 2.8 mgN g sediment 1) and those in seven groups of worms fed on high food concentrations (i.e. between 2.8 and 7.4 mgN g sediment 1) ( p < 0.05, Sokal and Rohlf, 1982). Thus, we also accept tentatively that the standardized relationship of the ingestion rate is reasonable sensitive and is suitable to determine the nutritional condition in the field.

7. Sediment nutrient for the field sediments and the nutrient available in the mudflats of Taiwan 7.1. Growth rate experiment using field sediments In considering the field sediment treatments, it was found that all the concentrations were falling in the region of low food concentrations in the standardized relationship curve. This suggests that the sediment nutrients in the mudflats of Taiwan are relatively low level. The alternative explanation is that the nutrient availability was low from fall to winter. Cheng and Chang (1999) found that both the total organic nitrogen and bioavailable protein content (Coomassie Blue method, Mayer et al., 1986) in the mudflat of Chu-wei Mangrove Forest were low in the fall and winter. High summer heat and enhanced bioturbation activities may speed up exhaustion of sediment nutrients and resulted in low concentration of residual sediment during the sampling period. Similar seasonal change in sediment nutrients was also observed in a temperate salt marsh of New York (Cheng et al., 1993). Under the similar food concentration, some growth rates lied above the standardized regression line, while others dropped below this line. Growth rates from Haw-mei-laiu and Sie-tau sediments fell above the standardized regression line, while the rates from Ba-Li, Hon-mou, Shan-san and Wen-tou-je sediments fell below that

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line. The sites with higher growth rate suggest that the sediments may contain nutrients other than the chemical indicators measured in this study. The sites with lower growth rate suggest that the sediments may contain materials such as pollutants that interfered the nutrient absorption process, thus resulting in a decrease of the growth rate. Foss and Forbes (1997) found that under the exposure of 101 Ag fluoranthene g 1 sediment dry weight, Capitella sp. I decreased its growth rate by 50%. Furthermore, the growth rate of polychaete, Capitella sp. I decreased significantly when the sediment contained more than 74 Ag g 1 4-n-nonylphenol (Hansen et al., 1999). Hrong (1998) also found the growth of Capitella sp. I has retarded in contaminated sediments from Newtown Creek, New York, containing 34.5 Ag g 1 nine polycyclic aromatic hydrocarbons (PAH). An in-vitro experiment demonstrated the activities of digestive enzymes in the gut of numerous benthic invertebrates were inhibited by the additions of dissolved copper (Chen et al., 2002). Their findings may suggest a linkage between sediment pollutants and food absorption. Nevertheless, our approach may serve as a tool to examine the sediment quality, not only in terms of traditional chemical indicators, but also the potential growth retardation factors. Many growth experiments suggest that deposit feeders respond partly to increase of both TOM and TOC, while the sediment nitrogenous materials (e.g. amino acids) were the limiting factors (Tenore, 1977; Rice, 1982; Marsh et al., 1989; Tsytsynum et al., 1990). Recent studies further demonstrated that the EHAA has a closer relationship with the growth of deposit feeders than the TON in sediment (Hrong, 1998; Linton and Taghon, 2000). In addition, the EHAA has been suggested as a better candidate for the sediment nutrient than the other chemicals conventionally used for sediment quality (Hrong, 1998; Linton, 1999). Thus, we concluded that the EHAA is the better predictor for sediment quality and may serve as sediment nutrient for the growth of deposit feeders. Even so, TOC may also be a good indicator of sediment nutrients for the growth in this study. .

8. Ingestion rate experiment using field sediments For the field sediment experiment and the standardized experiment, under the similar EHAA concentrations, only one datum of the standardized experiment lied outside the confidence interval, while the others fell in the region of 99% confidence intervals. Ingestion rate from Sie-tau sediment was much higher than the regression lines of the standardized experiment. Sediment from most mudflats in Taiwan had the similar nutritional values for ingestion rate to the standardized experiment. The feeding behaviour of deposit feeders reflects the difference in the nutritional value of sediment (Forbes et al., 1994; Taghon and Greene, 1990). Tenore (1983) found that the ingestion rate of Capitella capitata was not affected significantly by the change of food quantity. The nitrogen supply of detritus, on the other hand, had more significant influence. Forbes et al. (1994) found that the ingestion rate of Capitella sp. I increase with the nitrogen content of sediment. Horng and Taghon (1999) further demonstrated that the ingestion rate of this animal varied with the sediment EHAA contents. Linton (1999) also proved that the EHAA is the major influential factor to the feeding behaviour of deposit feeders, such as Capitella sp. I. The result of this study supports their conclusions.

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We conclude that EHAA is the better candidate of the sediment nutrient for deposit feeders.

9. Influence of energy absorption to the resource allocation in deposit feeders In the standardized growth experiments, a few animals were found mature and containing eggs in the very low nutrient concentrations (e.g. TON from 0 to 0.15 mgN g sediment 1). These phenomena were not found in animals fed with higher food levels. The size of these mature animals in the lower nutrient conditions was smaller than the ones reared in the higher food levels. Because the animals for this experiment were started with immature subadults, the early maturation under the low food concentrations can be explained by the relocation of available energy in animals in response to the change of their food environments. In the low food environment, animals tend to stop growth, relocate its available energy to reproduction and try to mature earlier. Furthermore, they may speed up their reproductive process to increase the total number of offsprings, thus produce the eggs earlier (Calow et al., 1979). This energy relocation phenomenon is common among marine invertebrates (Sebens, 1979). Similar phenomena were observed when the animals exposed to the high concentration of pollutants such as 4-n-nonylphenol (Hansen et al., 1999). However, it is possible that most animals were not able to carry out this energy relocation process, some even resulted in death, if the food simply was too low. Population of Capitella sp. I disappears from the field when the organic concentration drops below the threshold for the reproductive requirements (Linton and Taghon, 2000).

10. Capitella sp. I as an indicator species for the sediment nutrients Capitella sp. I is widespread in polluted estuaries and mudflats with high organic content, and is used as an indicator species for the environmental pollution (Grassle and Grassle, 1974; Reish, 1979; Pearson and Rosenberg, 1978). The reported sediment organic nitrogen content in the mudflats and estuaries of Taiwan ranged from 0.2 to 4.8 mgN g sediment 1(Chang, 1994; Chen and Lin, 1996; Hwang, 1998; Kuo, 1998; Fang, 2000; Liu, 2000; Chen, 2001). These sites include the estuaries that are heavily polluted by the organic toxicant, such as polychlorinated biphenyls (PCBs) (Chen and Lin, 1996) and urban pollution, such as household and industrial waste discharges (Yang, 1994). In this experiment, Capitella sp. I was found responded both at the ingestion and growth rates to the change of food concentrations. The sensitivity of the feeding physiology to the small change in the food environment and the deposit-feeding nature of Capitella sp. I allow our method to be a viable bioassay approach to the sediment nutrient in the field. In spite of this conclusion, both the ingestion and growth rates of the field sediments varied more than the laboratory-controlled sediments. These results suggest that the field sediments may contain the substances that can influence the energy uptake (ingestion) and absorption (growth) of the animals. These materials include bioavailable nutrients other than the EHAA, or deterrent substance such as heavy metals and organic pollutants. It is of

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interest to know the effect of pollutants to the physiology or energy transfer within the animals. Most of the estuaries and mudflats in Taiwan are polluted by industrial, urban and agricultural pollutants. In the future studies, it is recommended that one should include the effect of potential polluted materials, such as heavy metals, to the energy uptake and absorption of the animal in order to determine the influence of different exotic material on this bioassay approach. Finally, the combination of bioassay approaches and sediment analyses such as EHAA concentration, grain size characteristic, and toxic substance concentrations will allow us to further determine the availability of the sediment to the animals.

Acknowledgements The authors would like to thank Mr. H-C. Lin, J-S. Hwang, J-T. Hwang, Y-H. Dwan and Ms. C-J. Hwang for their assistance in the field and laboratory works. We also thank Mrs. J. Grassle for sharing her polychaete cultures. This study was partly supported by grants from the National Science Council, NSC91-2313-B-309-001, and NSC92-2313-B309-001. [SS]

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