ELSEVIER Journal of Experimental Marine Biology and Ecology,

202 (1996) 107-l 18

JOURNAL OF EXPERIMENTAL MARINE BIOLOGY AND ECOLOGY

The role of the burrow funnel in feeding processes in the lugworm Arenicola marina (L.)

A.S.W. Retraubun, M. Dawson, S.M. Evans*

Department of Marine Sciences and Coastal Management, lJniversit,y of Newcastle upon Tyne. NE1 7RU, UK

Received 29 March 1995; revised 21 December 1995; accepted 31 January 1996

Abstract

Lugworms (Arenicoh marina) are typical marine deposit feeders (Jumars, 1993). Labile organic

matter, notably bacteria, meiofauna and diatoms, is digested from the large volumes of

nutritionally-poor sediment which are processed by the gut. Detritus is not evidently digested. However, it is trapped in the funnel of the burrow, and probably enhances the nutritional quality of the food by providing a substrate for bacterial growth. The worm’s irrigation current is also

important because, if the headshaft of the burrow is blocked so that the current no longer reaches

the funnel, there is a decrease in the numbers of bacteria there.

Keywords: Lugworms; Arenicola marina; Feeding

1. Introduction

Feeding strategies of marine deposit feeders, with the notable exceptions of the snail

Hydrobia, and the fiddler crab Uca, are poorly understood (Jumars, 1993). This is even the case, for instance, in the lugworm Arenicoh marina (L.) which has been relatively intensively studied. Lugworms inhabit characteristically U-shaped burrows and have a

substantial impact on the sediment by reworking it. Large volumes of this nutritionally poor food are ingested from the feeding pocket, which is at the base of the headshaft of the burrow, and the undigested remains are subsequently deposited as faecal casts on the

surface, adjacent to the exit of the tailshaft. The diet itself has been subject to considerable debate. Thamdrup (1935) suggested that the worms fed unselectively on organic matter delivered to it via the headshaft of the burrow; Hylleberg (1975) thought

*Corresponding author.

0022-0981/96/$15.00 0 1996 Elsevier Science B.V. All rights reserved

PII SOO22-098 1(96)00017-2

108 A.S.W. Retraubun et al. I J. Exp. Mar. Bid. Ed. 202 (1996) 107-118

that meiofauna were the main source of food but that worms also benefitted from the direct uptake of nutrients; and Cad&e (1976) and Rijken (1979) suggested that diatoms were important food items. More recently, evidence has accumulated that bacteria form a substantial part of the diet (Boon et al., 1978; Rijken, 1979; Grossman and Reichardt,

1991). Any mechanism which enhanced the nutritional quality of the food would be

beneficial and the suggestion by Hylleberg (1975) that A. marina “gardens” by culturing meiofauna in the headshaft of the burrow attracted considerable interest. He

proposed, on the basis of observations of Abarenicolu spp., that high nutrient levels at

the base of the headshaft (from the lugworm’s excretions, decaying plant matter and

diffusion from the surrounding anoxic area), coupled with the supply of oxygen from the irrigation current, stimulated bacterial growth. This increased microbial content then attracted large numbers of nematodes, flagellates and ciliates, which were consumed and digested by the lugworm. Rijken ( 1979) argued that gardening could not occur in A.

marina burrows because ingestion rates of headshaft sediment were too fast to allow for

significant growth of bacteria. However, Hylleberg (1975) believed that a feeding pause of 6 h would be sufficient to allow doubling of many bacteria, and he had observed a suspension of feeding in Aburenicolu p@ficu for periods of as much as 24 h. Similarly,

Cadee ( 1976) described periods of up to five days in which A. marina did not feed.

There has also been disagreement on the definition of gardening. Hylleberg (1975) originally described it as the process of stimulating growth of bacteria, nematodes,

flagellates and ciliates and their subsequent use as food. Similarly, Grossman and Reichardt (1991) considered it to be any growth-promoting effect of burrowing macrofauna on copiotrophic sediment bacteria. However, Plante et al. (1990) suggested

that the nutritional benefit must be from direct consumption of increased microbial abundance and not mediated through the food web (termed “kitchen garden(ing)” by

Fenchel and Finlay (1989)). The objectives of the present study were to: (i) determine the principal components of

the diet of A. marina by taking samples of sediment from stages in its passage along the burrow system and worm’s digestive tract; and (ii) investigate the role of the funnel of

the burrow in enhancing growth of food organisms.

2. Methods

The study was carried out in 1993 and 1994. Field studies were made on a population

of A. marina inhabiting the shore at Goswick Sands, Lindisfarne (Northumberland). It is a low energy shore which supports a large permanent population of lugworms. Worms used in laboratory studies were also collected from this site.

Measurements of the dimensions of burrows and related structures were made in October 1993. Burrows were prised open by inserting a spade into the sediment about 10 cm either from either the headshaft or the tailshaft. The sediment tended to sheer across the burrow’s shafts as pressure was applied to the spade’s handle. In addition, redox potentials were measured using a Jenway 3071 pH meter with appropriate probes. They were measured at 2 cm intervals (n = 10 in each category): (i) vertically down the

A.S.W. Retraubun et al. I .I. Exp. Mar. Bid. Ed. 202 (1996) 107-118 109

headshaft of the burrow, (ii) vertically down sediment approximately 10 cm from the

burrow, (iii) horizontally across sediment and the headshaft of the burrow at a depth of

about 10 cm below the surface and (iv) horizontally across the surface sediment

including the funnel of the burrow.

Diet was investigated by measuring changes that occurred in the organic content of sediment as it passed through the burrow system and the worm’s gut. Samples of sediment (n = 10 in each category; see Table 1) were collected in November 1992 by

using a spatula. As far as possible, samples were restricted entirely to the part of the burrow indicated (funnel or headshaft) and were not contaminated with any surrounding sediment. Each sample consisted of about 5-10 g of sediment. Foregut samples were

taken from worms (n = IO) which had been killed by plunging them into boiling water. All samples were processed within 24 h of collection. Procedures for treating them are

described below.

2.1. Diatoms

Diatoms were extracted from 1 g sediment subsamples (one from each sample) on glass microscope slides by covering them first with filter paper and then a glass cover

slip. These samples were left overnight under illumination. Light was provided by a standard 60 W bulb in a bench lamp 30 cm above the slides. Diatoms migrated upwards

and became attached to the cover slip. The following morning coverslips were removed, mounted on clean slides and the numbers of diatoms in ten microscopic fields of view

(magnification X 400) counted for each of them.

2.2. Maiofauna

1 g subsamples of sediment (one from each sample) were flooded with solutions of magnesium chloride in order to anaesthetise the meiofauna, which were then preserved and stained with Rose Bengal in 4% formalin in seawater. They were stirred in a

magnetic stirrer for 10 min, and the supernatant liquid filtered through a 63 km sieve.

This procedure was repeated three times for each sample. Counts were made of meiofauna in the sediment, observed under a binocular microscope.

2.3. Detritus

Subsamples of approximately 1 g (one from each sample) sediment were immersed in seawater in petri dishes and observed under a binocular microscope. Pieces of detritus were picked out of them during ten one-minute searches. Subsequently dry weights of

extracted detritus were measured.

2.4. Bacteria

Plate counts of aerobic heterotrophic bacteria were obtained on a marine agar

containing 0.7 g of neopeptone, 0.2 g of glucose, 0.1 g of yeast extract and 1.5 g of agar in 1 litre of artificial seawater. Using a plate spread technique, 0.1 cm3 portions of serial

Tab

le

1 N

umbe

rs

of

diat

oms,

m

eiof

auna

, ba

cter

ia

and

amou

nts

of

detr

itus

in

vari

ous

part

s of

th

e A

. m

arin

a bu

rrow

an

d re

late

d st

ruct

ures

Posi

tion

Det

ritu

s D

iato

ms

Tot

al

mei

ofau

na

Plat

ed

bact

eria

T

otal

ba

cter

ial

coun

ts

X I

O’

(g/g

se

dim

ent

X I

O-‘

) (g

-l)

(g-l

) N

umbe

rs

Tax

a di

vers

ity

Surf

ace

sedi

men

t 1

I.05

4.

8 1.

650.

9 51

.4k2

.8

30.7

5 13

.3

12.6

kO.5

10

4+

3 Fu

nnel

43

.3”

11.9

1.

720.

4 57

.0t5

.1

36.8

t 9.

2 13

.8k0

.9

243k

ll H

eads

haft

(1

0 cm

de

pth)

12

.92

2.1

1.52

0.4

14.O

kO.7

42

7 t

307

12.7

kO.5

18

2t15

A

. m

arin

a fo

regu

t 14

.62

4.0

5.72

2.5

- 78

80

k409

2 4.

720.

9 _

Faec

es

28.7

2 9.

0 2.

22

1.5

9.4k

O.4

12

4 2

43

9.32

1.3

1072

60

Ano

xic

sedi

men

t ( 1

0 cm

de

pth)

10

.4+

4.2

0.4k

O.2

41

.7Z

0.2

5.O

k 3.

0 5.

850.

5

Mea

ns

are

pres

ente

d 2

thei

r st

anda

rd

erro

rs.

In t

he

case

of

m

eiof

auna

, sa

mpl

es

of

cast

s w

ere

take

n im

med

iate

ly

afte

r th

ey

had

been

de

posi

ted.

A.S.W. Retraubun et al. I J. Exp. Mar. Bid. Ed. 202 (1996) 107-118 III

solutions of sediment suspensions ( 1 g sediment shaken in 10 cm3 of water) were

applied to the agar in duplicate. Colonies of bacteria were counted after 3 wk of

incubation at 25°C. The most frequent bacterial types were identified on the basis of the

shape and colour of colonies, and standard Gram stain, catalase and oxidase tests. In view of the paucity of information on marine bacteria, no attempt was made to identify

individual taxa. Total bacterial counts were made from 2 cm3 sediment subsamples (one from each

sample) taken with a plastic syringe. They were preserved on collection in 2% formalin in filtered seawater. The sample was shaken by hand, put into a universal sterile bottle and 10 cm3 of 0.1% sodium cholate was added, together with 5 glass beads (2.0-3.0

mm in diameter) and 2 cm3 of dewex. The sample was shaken in an orbital shaker at 100 t-pm for 2 h, and then centrifuged at 2500 rpm for 10 min. 1 cm3 of the supernatant fluid was placed in an eppendorf tube and microfuged at 1300 rpm for 10 min, before 0.3 cm3 of the detergent NP-40 (in PBS) was added. Three 0.5 cm3 subsamples were taken and placed on gelatin-treated slides. They were dehydrated successively in 50, 80 and 95%

ethanol, allowing three min for each treatment. Numbers of bacteria were counted, using

an epifluorescent microscope, after staining them with 0.01% acridine orange. Counts were made in ten microscopic fields for each subsample at a magnification of X 1000.

A field experiment was carried out to investigate the effects of preventing the lugworm’s irrigation current from reaching the sediment in the funnel of the headshaft of

the burrow on the growth of bacteria in it. This was done by pushing Perspex sheets 10 cm X 5 cm, obliquely into the sediment adjacent to burrow funnels so that they cut across the headshaft separating the funnel from the rest of the burrow. There were eight experimental burrows and eight controls which were not treated in this way. Experimen-

tal and control burrows were paired on the basis of their proximity to one another. Sediment samples were taken for total bacterial counts from the funnels of burrows of

both experimental and control groups when the experiment was set-up and approximate-

ly 48 h later. Means are quotedktheir standard errors (SE.) throughout this paper. Unless stated

otherwise, the t-test has been used to determine levels of significance between means.

3. Results

The headshafts of A. marina burrows were characterised by cone-shaped depressions forming funnels in the surface sediment, and the tailshafts by mounds of faecal casts

(Fig. 1). Although these surface structures were often destroyed by wave action, they had a substantial impact on the topography of the surface during calm weather. Algal debris, such as pieces of frond or thallus of macroalgae, tended to collect in the funnels. The dry weight of algal debris collected from them (X = 0.0163+0.0020 g per g

sediment, n = 22) was significntly greater than that from equivalent areas of surface sediment 10 cm away from burrows (X = 0.0008-+0.0003 g per g sediment; n = 22) (P < 0.001, Wilcoxon matched-pairs signed-ranks test).

Headshafts of burrows extended deep into the dark anoxic sediment but, since they were usually filled with the light coloured sediment from the surface, they were

112 A.S.W. Retraubun et al. I J. Exp. Mar. Biol. Ecol. 202 (1996) 107-118

RPD _ I_---_ ---------a_- -m

ts -

- hs 0.33*0*03

0~35*0~03

__

21.0 27.6

Fig. I. Measurements (n = 10 in each case) of various parts of the burrow system of A. marina. Abbreviations:

f = funnel; hs = headshaft; fp = feeding pocket; hg = horizontal gallery; ts = tailshaft; fc = faecal cast; RPD =

redox discontinuity layer.

conspicuous when burrows were prised open (see Section 2). The surface sediment had high redox potentials, which declined gradually with increasing depth beneath the

surface, until the Redox Potential Discontinuity layer (RPD), the boundary between the light coloured surface and the dark anoxic sediment, was reached. Here redox values

decreased rapidly with increasing depth (Fig. 2). Redox values in burrow funnels were higher than those in adjacent surface sediment. They were also higher down the headshaft of the burrow (remaining at surface levels) than in adjacent sediment (Fig. 2).

Sediment in the study area was rich in diatoms, meiofauna, detritus and bacteria, all of

which were potentially available as food for A. marina. Evidence that they were utilised as such is as follows:

3.1. Diatoms

Diatoms belonging primarily to the genera Navicula, Rhizoselenia, Raphoneis,

Amphora, Nitzchia and Caloneis were common in surface sediment. They were

evidently transported down the headshaft of burrows with the descending column of sediment because they were present at similar densities in samples from the headshaft as

in those from the funnel and surface (Table 1). There is evidence of selective ingestion by the worms because the density in the foregut was significantly higher than that in the headshaft of the burrow (P < 0.05). There was a decline in the abundance of diatoms between the foregut and faecal casts. Furthermore, most diatoms in casts were empty, the contents evidently had been digested.

A.S.W. Retraubun et al. I J. Exp. Mar. Bid. Ed. 202 (1996) 107-11X

Depth profales Horrzontal profiles

200 1 WDown redlment l(c) locm below surface

2oo 1 (bIDown headshaft

Redox 100

In”

0 5 10

Depth (cm)

3210123

(d)At surface

20 10 0 10 20

Distance from burrow(O)(cm)

II3

Fig. 2. Mean redox potentials at various positions in the headshaft and funnel of the burrow and in adjacent

sediment. (a) Vertical profile in sediment, (b) vertical profile down headshaft of burrow, (c) horizontal profile at

10 cm depth across headshaft of burrows, (d) horizontal profile at surface across funnel of burrow.

3.2. Meiofauna

Copepods, nematodes, ciliates and ostracods were the most numerous members of the meiofauna in the surface sediment but gastrotrichs, turbellarians and polychaetes were also recorded in substantial numbers (Table 2). Meiofauna originating from surface

sediment were unlikely to have been a major component of the diet, however, because relatively few of them were transported down the headshaft of the burrow. Nevertheless,

Table 2

Numbers (means ? standard errors, II= IO) of meiofauna (g ’ sediment) in major taxonomic groups taken from

A. marina burrows and related areas

Group Burrow

Funnel Headshaft( 10 cm depth)

Sediment depth Cast

Surface IO cm

Ciliata 2.92 1.2

Copepoda 42.322.1

Gastrotricha 0.620.2

Nematoda 4.92 I .4

Ostracoda 3.91 I.5

Polychaeta 0.320.2

Turbellaria 2.120.8

Total 57.025. I

1.8+-I.2

4.l?l.l

0.220.2

5.52 1.6 I .9?0.8

0.3kO.3

0.220.2

14.OkO.7

9.0*4.4

11.9+1.7

0.lto.I

22.7k7.0

4.6+ I.2

0.620.3

2.551.1

51.4+-2.8

I .9%0.8 0.7 kO.4

0. I 50. I 1.2-tO.5

0 0

4.1*1.4 3.720.8

0.2”0.2 1.7?l.l

0.21-0.2 0.220.2

1.0+0.1 1.820.6

7.520.5 9.420.4

114 A.S.W. Retraubun et al. I .I. Exp. Mar. Biol. Ecol. 202 (1996) 107-118

a significant decrease in numbers of meiofauna in the faecal casts compared with the

headshaft suggest that some of those present were digested (Table 1).

3.3. Detritus

At least some of the organic debris which collects in the funnels of burrows (see above) became incorporated into the sediment in the funnel. This was because there

were significantly larger quantities of it in samples of sediment from funnels than in those from surface sediment nearby (P < 0.02, Table 1). The detritus was not transported down the headshaft in substantial quantities because samples from the headshaft were

poorer in it than those taken from funnels (P < 0.01).

3.4. Bacteria

Bacteria are almost certainly a major source of food for A. marina. There is also evidence that they are cultured in burrows. This is as follows:

1. Bacteria were numerous in surface sediments, particularly that which was rich in detritus. Numbers of (plated) bacteria correlated with the amount of detritus in

sediment samples from both burrow funnels and nearby surface areas (Fig. 3).

Funnels acted as traps for detritus (see above) and, as would be expected if they were used as substrates for growth, bacteria were more abundant in funnels than in other

parts of the surface sediment (f’ < 0.01, Table 1).

Bacteria

x 10’ 0.004 0.008

. Futlnel rro~ss’ .

. .’ * 1

0.005 0 01 O-015 0 020

Detritus (g per g sediment)

Fig. 3. Spearman Rank correlations between numbers of plated bacteria and detritus in samples of (a) surface

sediment and (b) sediment from funnels of burrows. *P < 0.05.

A.S.W. Retraubun et al. / J. Exp. Mar. Bid. Ed. 202 (1996) 107-118 I15

2. Bacteria were evidently transported down the headshaft of the burrow with the

descending sediment, because densities (total counts) of them in headshafts were high

and not significantly different from those in funnels (P > 0.05, Table 1). Furthermore,

the population of bacteria in the headshaft was apparently the same as that at the surface. A total of 20 bacterial taxa were identified by plating techniques and each was recorded in samples from the headshaft, funnel and surface sediment (Fig. 4).

They were also recorded in similar relative proportions of abundance at each of these sites. The Kendall coefficient of concordance for their rank orders of abundance at them was 0.9022 (P < 0.001). The diversity of bacteria (i.e., number of taxa) was

also similar in samples taken from these places (i.e., numbers of taxa, Table 1). 3. The population of bacteria in the anoxic sediment was different from that in the

surface sediment (and almost certainly included anaerobic species which were not

identified by the plating techniques used here). The Spearman rank coefficient of

correlation between the rank orders of abundance of taxa in anoxic and surface

sediments was 0.3 122 (P > 0.05).

4. Bacteria were evidently digested in substantial numbers because abundances of plated bacteria in samples taken from the ingestive side of the burrow system (headshaft or foregut) were much higher than those on the egestive side (faecal casts, Table 1). Similarly, counts of total bacteria from the headshaft were higher than those from the

faeces.

Percent Head shaft I

of lb&

population

Anoxic sediment

5 i0 Ii 21 Taxon number

Fig. 4. Relative proportions of twenty bacterial taxa at different positions in the burrow system of A. marina.

116 A.S.W. Retraubun et al. / J. Exp. Mar. Biol. Ecol. 202 (1996) 107-I 18

Table 3

Mean numbers (5standard errors) of bacteria (total counts), in samples taken from the funnels of burrows

(n = 8 in each case) before and after the headshaft had been blocked by the insertion of a plastic sheet

Sample group Number of bacteria X 10’

Before After

Experimental

Control

187.8+12.4 135.4k7.6 P io.01

208.5? 6.3 21.5.0Z6.3 n.s.

Controls did not receive this treatment. Statistical comparisons were made using the Wilcoxon matched-pairs

signed-ranks test. n.s. = not significant.

There is evidence that the worm’s irrigation current is important in maintaining the

abundance of bacteria in the headshaft. There was a significant decrease in the density of bacteria in funnels of burrows 48 h after the insertion of a plastic sheet between the funnel and headshaft, but no significant change in densities in controls over the same period (Table 3).

4. Discussion

Feeding in the lugworm is characteristic of that of marine deposit feeders (Jumars,

1993). Large volumes of nutritionally-poor food (sediment) are processed in the gut, but since its residency time in the gut is short, only labile organic matter can be digested.

There is insufficient time to digest refractory components of the food. The throughput of sediment in A. marina is 4.7-80 cm3 per day (Cadee, 1976) and the residency time in

the gut is about 15 min (Kermack, 1955). Bacteria and diatoms are components of the diet because their numbers decreased during their passage through the gut (see also Grossman and Reichardt ( 1991)). They were also effective foods when they were supplied as artificial diets in the laboratory. Rijken (1979) found that either bacteria or

diatoms enhanced the growth of lugworms which were fed on them. Meiofauna trapped by the funnel, and then transported down the headshaft to the feeding pocket, are unlikely to form a significant part of the diet because they occur in such low numbers in

the headshaft. They probably escape ingestion by migrating upwards against the flow of the descending column of sediment. Nevertheless, a rich (and probably self-sustaining)

population of meiofauna occurs in the feeding pocket (Scherer, 198.5), and this is presumably ingested by lugworms. Detritus is evidently not digested and, since

lugworms do not secrete cellulase (Longbottom, 1970) it probably passes largely unaltered through the gut. Minced Ulva, fed to lugworms as artificial detritus, was utilised ineffectively by them (Rijken, 1979).

Pits in the surface substrate are sites of selective deposition of particles of low specific gravity (Yager et al., 1993). They could therefore improve the diets of deposit-feeding benthic organisms such as A. marina by, for example, trapping organic matter, including bacteria and/or detritus. Indeed, it was shown here that algal debris is trapped by the funnels of A. marina burrows. Its effect is evidently indirect, because although it is not digested, it probably forms a substrate for bacterial growth in the burrow system. As

A.S.W. Retraubun et al. I J. Exp. Mar. Bid. Ed. 202 (1996) 107-118 117

would be expected if this is the case, bacteria were present at higher densities in the

funnel than in adjacent sediment. This could be due to selective deposition of bacteria in the funnel but the reduction in the quantity of detritus between the funnel and headshaft

suggests that it is being utilised by bacteria. Furthermore, when the worm’s irrigation current was prevented from reaching it by inserting a Perspex sheet into the headshaft, the numbers of bacteria growing there decreased. This current, which involves the passage of about 40 cm3 of oxygenated water h-’ through the burrow in a posterior- anterior direction (Baumfalk, 1979) effectively extends the RPD layer deep into

otherwise anoxic sediment. It creates highly favourable conditions for the growth of

bacteria and the meiofauna which feeds on them (Scherer, 1985; Andersen and Kristensen, 1992; Kristensen et al., 1992). This system by which the lugworms trap indigestible detritus and then convert it into digestible bacteria (and/or meiofauna which consume the bacteria), can be described as “gardening” according to any of the

definitions which have been used previously (see Section 1). Selective ingestion of nutritive particles by the lugworm is an additional means of

improving the quality of its food. Baumfalk (1979) showed that small particles are

ingested at the expense of larger ones, which collect at the base of the headshaft, often forming a recognisable layer there. These small particles evidently include bacteria

which are present in the foregut in larger numbers than in the sediment of the headshaft (Grossman and Reichardt, 1991; present investigation). Similarly, diatoms appear to be ingested selectively because they too are concentrated in the foregut.

Biogenic structures, such as those created by A. marina burrows, have substantial impacts on the “neighbouring” interstitial fauna (e.g., Reise and Ax, 1979; Reise, 198 1;

Scherer, 1985). As Reise (1981) had shown earlier, the meiofauna inhabiting the funnels of A. marina burrows and casts differ from those occurring in nearby surface sediment. Recently-deposited casts are poor in meiofaunal abundance (present study), although

organisms undoubtedly invade them as they age (e.g., Reise, 198 1; Reise, 1985). It was shown both here, and by Reise (1981) that copepods aggregate in funnels which represent tiny pools when the tide is out; nematodes tend to avoid funnels and casts.

Acknowledgments

ASWR would like to express his thanks to the Indonesian Government’s Marine Sciences Education Project for funding. He also thanks the former Rector, Professor J.L.

Nanere, the former Dean of Fisheries Mr J.M. Nanlohy and the present Rector, Dr M. Huliselan, of Pattimura University (Indonesia) for their constant support and encourage- ment. Thanks are also due to Dr A.G. O’Donnell for his help in estimating numbers of bacteria.

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