Variation in paragnath number in some British populations of the estuarine polychaete Nereis diversicolor

Estuarine and Coastal Marine L%ence(1977)

5,77x-781

Variation in Paragnath Number in Some British Populations of the Estuarine Polychaete Nereis dizmsicolor

R. S. K. Barnes

and S. M. Head”

Department of Zoology, University of Cambridge, Cambridge, U.K. Received6 August 1976 and in revisedform 12 February 1977

Keywords: morphology

estuarine habitat, polychaeta,

taxonomy,

population

variations,

Paragnath variation was examined in four populations of N. diversicolor differing markedly in the nature of their habitats. The basic pattern of paragnath numbers and distribution is described and discussed. Paragnath groups I to IV (inclusive) are highly correlated and appear to vary as a symmetrical unit, whilst groups VI and VII-VIII vary both independently of each other and of groups I-IV. Populations differ from each other in the mean number of paragnaths in the various groups, but not in the extent of variation about those means. Intra-population variation is not a result of variation in size of the worms, and it appears to be essentially unimodal in

all paragnath groups. This pattern of variation is discussed.

Introduction Following

the early work of J. G. H. Kinberg

on the genus Nereiq systematists and ecologists

have been interested in the distribution and abundance of the cbitinous paragnaths borne on the eversible section of the buccal tube (the ‘proboscis’). These denticles are disposed in two belts : an anterior one (posteriorly situated when the proboscis is fully everted) of simple cones or forwardly directed, sickle shaped teeth, and a posterior one of long, strongly curved teeth directed backwards and towards the lumen of the gut. The posterior paragnaths presumably ensure that material seized by tbe jaws is taken into the gut on retraction of the proboscis, includiig prevention of withdrawal by active prey. The function of the anterior paragnaths is concerned with burrowing or browsing on the sediment surface: when engaged in either of these activities, Nereis only everts the anterior belt (Dales, 1963), the paragnaths of which then rasp the substratum. Paragnaths are lost or are shed from time to time and replacement is effected by secretion from the stomodeal epithelium (Kaestner, 1967). Amongst Nereis spp., N. dive&color 0. F. Miiller is particularly variable in the numbers of individual paragnaths comprising the various ‘groups’ recognized by Kinberg (Figure I); it is, for example, more variable than the more marine and more predatory N. virens and N. succinea (Muus, 1967). Variation in paragnath number in populations of N. diversicolor from eight Danish, two Swedish and one Finnish localities was investigated by Muus (1967). We-sent address: Department of Zoology, University of Oxford, Oxford, U.K. 77x

772

R. S. K. Barnes & S. M. Head

-

XI (left)

Figure I. Camera-lucida drawing of (a) the dorsal surface and (b) the ventral surface of the everted proboscis of a Nereis diversicolor from Fawley, showing the paragnaths grouped according to the system of Kinberg.

He found much intra- and inter-population variation and showed that this did not result from a relationship between size of worm and paragnath number; for example, a series of worms showed a mean number of paragnaths in group VII-VIII of c. 27 regardless of sex and of size within the Iength range of 45-92 segments (Muus, 1967, Figure 41). In respect of inter-population variation, Muus concluded that N. diversicolor, which has a non-pelagic larval phase, is divided into a series of local ‘races’ which have diverged from each other in paragnath number for unknown reasons. He failed to find any obvious environmental correlates of paragnath number, except that he considered the reduction in numbers of paragnaths in some groups, e.g. I, in populations from low salinities to be a potential example of the frequently observed reduction in the units comprising meristically-varying characters of euryhaline animals from the less sahne end of their salinity range (see e.g. Barnes, 1974). The causes of the high intra-population variability displayed by N. diversicolor remained, and remain, mysterious. It was, therefore, the object of this study to investigate and compare variation in paragnath number in populations of N. diwersicolor from representatives of the range of habitats

Purugnuth wariation in Nereis diversicolor

773

occupied by this species in southern Britain, particularly with respect to potential causes of this variation. The four localities sampled in this survey were: the sandy banks of the Gann Estuary draining into Milford Haven, Dyfed (SM 814075); the muddy-sand banks of Mow Creek on the Brancaster Marshes, Norfolk (TF 794447); the soft-mud sides of a tributary of the Test Estuary at Eling, Hampshire (SU 366126); and the soft and glutinous mud forming the sides of a creek in the Spartirza marshes between Fawley and Calshot, Hampshire (SU 478026), some 15 km down Southampton Water from the Eling site. These localities can be characterized, respectively, as (a) brackish and sandy, (b) marine and sandy, (c) brackish and muddy, and (d) marine and muddy, and include populations from the Atlantic, the North Sea and the Channel. The Fawley site near the mouth of Southampton Water was visibly polluted by oil which had soaked into the mud in which the Nerei> were living. The possible relationships between paragnath numbers and various features of the habitats of Nereis will be considered in a later paper. Methods From 70 to 120 worms were dug from a limited area (<0*75 m2) at each site and were transported, live, to an adjacent laboratory, namely Orielton Field Centre (Field Studies Council), Dial Cottage (Nature Conservancy Council) or the C.E.R.L. Marine Biological Laboratory. Live worms were persuaded to evert their proboscis by dipping them in 95% alcohol; they then died usually with the proboscis everted. A few specimens died with the proboscis totally or partially retracted, but this was easily remedied by generating pressure some distance behind the head. In the samples collected and processed first (those from Dyfed and Norfolk), the distance from the tip of the prostomium to a line joining the anterior margin of each of the anterior pair of eyes was measured immediately after death, the number of setigerous segments was counted if the worm was intact, and the number of paragnaths in each group was assessed(the scar left by the recent loss of a paragnath was scored as if that paragnath was still present). Worms were maintained alive until required for paragnath assessment, the process of counting and measuring a sample taking some 3 days during which time no worms died naturally. After confirmation of the unimportance of size of worm in respect of paragnath number in any group, length measurements were discontinued and the later samples (i.e. from Southampton Water) were merely collected from the field, preserved with the proboscis everted, and stored for later assessment of paragnath number at a convenient time. Worms were collected from the Gann Estuary on 31 March 1976, from the Brancaster Marshes on 30 May 1976, and from the two sites in Southampton Water on 6 July 1976. The collected data were processed by an IBM 3701165 computer using the ‘NTSYS’ Numerical Taxonomy package of Rohlf et al. (1974) for product-moment correlation, pair-group clustering and principal component analyses. The same computer was used to calculate analyses of variance and Mann-Whitney U, for which purpose various FORTRAN programmes were written. The basic pattern Although highly variable in number from worm to worm, in each worm paragnath number and distribution is nevertheless referable to a basic pattern comprising certain groups of dent&s with consistent intergroup symmetry and correlation (Figures I and 2, Tables I and 2).

R. S. K. Barnes

774

left

-

& S. M. Head

right

left

YIszIs!II left right

right

SZUI

0.8 ’

0.7 .

0.6 .

o-5

04.

0.3 *

0.2 * Figure 2. A phenogram of the inter-relations of the various paragnath groups, derived by an Unweighted Pair-group Averaging procedure from the productmoment correlation coefficients of the whole Nerek sample (Table I). The cophenetic correlation for this phenogram is very high, 0.983, so little distortion has resulted from simplification of the pattern of correlations. TABLE 1. Product-moment correlation derived from transformed (normalized) data on the various paragnath groups in the total sample of Nereis diversicolor”. Italicized values are significant at the P
111

IIr

III

IV1

IVr

0.16

VII

0.36 0.36 0’52 0.43 0.40 0.06

0.83 0.56 0’74 0.76 0.18

0.56 0.7’ 0.74

0.69 0.7r

0’21

0’12

0.86 0.16

0’11

0.13

0.14

0.13

0’11

0'12

0.80

0.27

0.16

0.17

0.28

0'12

0.13

0.17

VIr

0.17

‘Nonparametric correlations (Spearman and Kendall rank correlations) gave essentially very similar results, except in the case of group VI where anomalously low values were observed. This was presumably due to the large proportion of tied ranks, in the case of VI left ZIS.VI right in both the x and y variables, for which the programme used was not able to correct the results. The product-moment correlation matrix is considered a better representation of affinities, since the distributions approximate to normality and a normalizing transformation was used (x - 2))s.

Thus the ring of paragnaths surrounding the jaws is divided into six clusters: I, II left, IV left, III, IV right, II right. Of these, the numbers of paragnaths in each of the left-right pairs II and IV are not only very strongly correlated (Table I) but are also subequal, an individual worm differing in numbers of teeth in each portion of a paired group by an

Paragnathvmiation in Nereis diversicolor

775

TABLE 2. Mean differencea between symmetrical arrangement2 of paragnath groups and, parenthetically, mean differences as percenrages of the mean total numbers of paragnatha in the participating groupa Groups 1II:IIr 1Vl:IVr III+IVl:IIr+ IVr IIr+IVl:IIl+ IVr I+III: ave II+ IV VIl:VIr

Brancaster 1.58f1.37 (7.27) 2-45&z18 (7.64) 2'77f2.37

(576) 3.02f2.83

(SW

3.78f2.81 (7.16) w84*0*84 b.27)

2-s f 1’75

Vh4 2.27fr63

c+-68) 3'29f2'39

(4-M 2'95f2'34 (3.66) 6*76f4'92 (9.04) X-39&1*42 (13'78)

Eling

Fawley

I-97fr.67

I-57f1.28

(‘93

(7.671 I-87&a-11 (7'S) 2.59f2.32 (5'7d 2'49i2.42 (5'49) 3'79f344

2.87f2.35 (6.69) 3'77f3-6

(5.18)

3'3Of2'53 (4'53) 8.63 f6.01 (13.22) 1'43fI.25 (15'05)

@44)

0.95fo.86 b-72)

average of 16-2.9 paragnaths (Table 2). This bilateral symmetry on both the dorsal and ventral surfaces naturally results in further lines of symmetry: II left+IV left will be subequal to II right+IV right; and II left+IV right will be subequal to II right+IV left along axes passing through the lumen of the gut (Table 2). Further, groups I and III are strongly correlated (Table I) and the axis passing through these two groups is subequal in paragnath number to the various axes passing through groups II and IV--although more so in some populations than in others. The constituents of the posterior ring are therefore all highly correlated and the radial lines of symmetry passing through the gut are all subequal in total paragnath numbers. There is, however, a numerical advantage in favour of the ventral paragnaths of over 2 : I. Considering their function and their distribution in a ring around the gut, a symmetrical arrangement of the paragnaths seems appropriate, although the precise function of the system of symmetry described above, with its bias in favour of the ventral elements, is purely conjectural. A symmetrical arrangement of the anterior ring seems less appropriate to its described function and, indeed, apart from the bilateral symmetry displayed by the paired groups VI left and VI right, which are highly correlated and more nearly equal than any other paired group (Tables I and 2), little symmetry is evident. Groups VI and VII-VIII are very loosely associated, both with each other and with any of the groups in the posterior ring (Table I). As with the posterior ring, however, there is a large numerical advantage in favour of the ventral paragnaths, in this case in the order of 4-5 :I. This bias may well be appropriate to an organism grazing the surface sediment.

Inter-populadon

variation

Basic data on paragnath numbers in the four populations are set out in Table 3, whilst Table 4 lists the significant differences between these populations. Several points emerge from these data. Any one population differs significantly from the other populations in the mean values of most of its paragnath groups (41 out of the 54 comparisons being significantly different), although the variation about the significantly different means tends to be similar in all populations (only 8 of the 54 comparisons of vsriance yielding significant differences). Secondly, paragnath groups I to IV tend to behave as a block and separately from groups VI and VII-VIII: in respect of all the groups I-IV, the Gann population shows the largest

R. S. K. Barnes C5 S. M. Head

776

TABLE 3. Values of mean, variance and range in numbers of paragnaths comprising the various groups in different populations of Nereis diversicolor

I

111

IIr

III

IV1

15.96

10.92 16.06

14.82 IO.23

IS.05 10.24

23'93 31'19 26.73 20.23

15.80 23'87 21.38 12.40

7’13

7‘95

IVr

VII

VIr

VII-VIII

16.28 24.66

3.98 5.16 4'73 4'49

4.20 4.93 4'77 4'37

38.42 43'32 34'77 40.41

__~ f (Brancaster) R (Eling) 2 (Fawley)

2.05 3’32 2.13 I.99

so (Brancaster) sz (Gann) sz (Eling) s a (Fawley)

1’04 166 I.59 1’30

Range Range Range Range

o-- 6

,t (Gann)

(Brancaster) (Gann) (Eling) (Fawley)

Range (total)

IO.Cp

9.26 10.69

IO‘22

9'92 9.86

11.63 j-22

S--I') 8-25

o-6

8-23 5-22

6-23 9-24 3-23

07

5-25

3-24

1-6 O--7

16.39

x1.36

12.06

I.14

1’2j

x2.75 22’00

2'54 2.72

2.64

26.52 27'35

14'27 13.62 IS.44

2’25

1.82

1.56

25.60 41'44 49.56 54.76

1-6

z-8 I-9 o-8

25-56 30-59 22-55

1-8

17-68

o-9

I

13'32

1 j-34 20-4.5 17-40 12-34

IS-32 9.~32 3-23

8-26 X5-34 12-30 3-23

o-9 ~-8

12-45

3-32

3-34

O-IO

o-9

2-35

7-48

o-6

4-27

12-65

9--2j

TABLE 4. Statistically-significant differences of different paragnath groups in different Whitney U test, variances by F test; Pto.02)

I Means” Eling vs. Fawley Eling vs. Brancaster Eling vs. Gann Fawley vs. Brancaster Fawley vs. Gann Brancaster vs. Gann Variances Eling vs. Fawley Eling us. Brancaster Eling vs. Gann Fawley vs. Brancaster Fawley US. Gann Brancaster vs. Gann ‘Exactly

III

12.49

2j.19

3-25

Range in Muus (1967) Range in Smith (1958)

2~‘55

IIr

III

X

x

X

X

x

Y

X

I-IO

3.-34

O-IO

4--40

Iv12

9-72

8--33

1-9

24-60

bet&-een the means and variances populations (means by Mann-

IV1

IVr

r:

i. %

VI1

VIr

Y

x

VII-VIII

x

x

‘._

;,’

X

‘i

s

.i

X 4:

X

x

X

x

x

x

x

x

X

X

X

X

x

x

x

X

r:

X

X

x

x

X

x

X

x the same significance

distribution

7-68

x

is given by Student’s

t test

mean number of paragnaths, Eling the second largest, Brancaster the third largest, and Fawley the smallest (although the differences are not all statistically significant); yet the order of decreasing mean size of group VII-VIII is Gann: Fawley : Brancaster: Eling. Thirdly, Brancaster exhibits the smallest variances for every paragnath group, and all significantly different variances involve comparison with Brancaster. The comparison between Brancaster and Fawley in respect of the variance of group VII-VIII provides the only case of significantly different variances about means which do not differ significantly (at the P
--2626313437404346495256 --------273033363942454661

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4 6 6 IO 12 14 I6 1620 aTsiisJicTilez‘is

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Figure 3. Percentage-frequency

0

20

30

0

IO

20

30

Brancaster

6

1922

24

p

374043464962555661

I3 I5 17 ISa! 14 16 I6 2022

histograms

25263134

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of the variation

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sampled.

65 5457

l-l

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373941

14 16 16 2022242626 I6 17 19 21 2325272931

lli,ll,,lllII 2225 26 31 34374043464952 ----------_24273033363942454651

6 IO 12 ------------9 II I3

16 162022242626303234363640 -----_------17 IS 21 2325272931 3335

12 14 16 16 202224 I3 I5 17 19 21 2325

from the four populations

--4345 4446

6 IO --------9 II

01234567

Eling

-----------

0,234667

‘,obi

Gann

VIIVIII

VI

IV

III

II

778

R. S. K. Barnes & S. M. Head

would appear that the factors effecting differences in the mean number of paragnaths in different populations are not those affecting the levels of intra-population variation in paragnath number. In order to ascertain whether any of the inter-population variation might be correlated with the environmental conditions summarized as ‘sandy’ or ‘muddy’, ‘brackish’ or ‘saline’, a two-way analysis of variance was carried out. Significant correlations were obtained, but as only one sample was taken from each of the four extreme salinity/sediment combinations

-6 ;; H

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Figure 4. Plots on probability paper of the cumulative percentage-frequencies of paragnaths in groups II, III, VI and VII-VIII from Brancaster and Fawley. (Brancaster is the least variable of the four samples in respect of these groups, and Fawley the most variable.)

Paragnath variation in Nereis diversicolor

779

and as the labels referred to above are extremely vague, thii aspect was made the subject of a separate study which will be reported in a later paper. Intra-population variation In an attempt to analyse intra-population variation, three investigations were conducted: (a) correlation of paragnath numbers with size of the bearer, (b) a search for polymodal distributions within the overall variation, and (c) principal component analyses. Product-moment correlation coefficients of length of worm with the number of paragnaths in each group were almost always negative and always small. In the Brancaster population, for example, the coefficient averaged -0.10 and was significant for only two paragnath groups, both halves of paired groups (II right and VI left). We therefore do not consider length of worm (i.e. number of segments) to be an important effector of intra-population variation. Histograms of percentage frequency of paragnath numbers were plotted for each paragnath group (Figure 3), as were cumulative percentages of paragnath frequency on probability paper (Figure 4). We do not feel justified in interpreting any of these distributions as other than being single and unimodal, and regard any departure from a straight line in Figure 4 as being consequent on comparative smallness of sample (Harding, 1949). Curvature at the low regions of the distributions plotted on probability paper reflects the departure from normality of a distribution of meristic characters as the mean approaches zero; this is most marked in groups I and VI. Principal component analysis was conducted on the samples from Brancaster and Gann in an attempt to locate clusters of worms with inter-related paragnath numbers. Such groups could arise from sexual differences or dietary specialization and would not necessarily be detected by analysing one paragnath group at a time. Using the matrix of product-moment correlations in Table I, three factor axes were extracted and the data for each individual worm projected on to them. These axes accounted for some 60% of the sample variance, but no clusters could be detected in the projected scattergrams, the data points proving rather evenly dispersed about the population centroid. It was concluded that the samples were homogeneous in paragnath numbers not merely within each group individually but also when analysed as a set.

Discussion Nerez.sdiversi~olor is a burrow-constructing animal which may inhabit the same burrow system for months (Schffer, 1972). It is therefore reasonable to assume that samples collected from very restricted areas comprise individuals which have been subjected to identical or very similar environmental conditions in the past. Variation amongst such individuals may then be the result of a number of causes, of which the following appear the most likely. (a) Variation with size or age of worm. Such a correlation might result from an increase in paragnath number with a proboscis of larger surface area (i.e. a positive correlation) or from an increasing loss rate with increase in age which cannot be made good by a decreasingly effective replacement rate (i.e. negative). (b) Variation with diet of a worm. N. divtmicolor possesses many different feeding modes (Barnes, 1974) which may require or affect different paragnath numbers. The circumstances triggering the different feeding modes are unknown, but it is conceivable that different individual worms have different preferential modes. In a habitat in which several modes could be used, such individual preferences could be expected

780

R. S. K. Barnes & S. M. Head

to give rise to (or result from) polymodal frequencies of paragnath number in the population as a whole. (c) Variation resulting from weakness of the selective forces acting on paragnath number. If N. diwersicolor has largely abandoned an active predatory role, several groups of paragnaths may be redundant and selection would not oppose variation or loss either of the ability to secrete paragnaths in certain areas or of the ability to replace those lost. (d) Variation resulting solely from the morphogenetic impossibility of secreting exactly the optimum number of paragnaths. Inter-population variation could be expected to result from: (e) Variation with some environmental feature such as sediment type or salinity, either via its effects on ‘ B ’ above or in some other fashion; or (f) (If ‘c’ above is the case), essentially random fixation or loss of the genetic determinants of paragnath pattern. Most other possible causes of variation approximate to one of the above types for current purposes. The results presented above suggest that (a) and (b), or any other factors either operating differentially on worms of different size or likely to result in polymodal frequencies, do not operate on the populations sampled. In respect of intra-population variation, it then remains to consider (c) and (d). If the variabilities tend not to differ significantly, then presumably either one factor is governing variation equally at each of the four widely separate sites or no factors are constraining variation which is to say that variation largely is selectively neutral and is therefore maximal. Excepting the constraint upon variation which must result from the system of symmetry evidently displayed by the paragnaths of groups I-IV, it is difficult to conceive of an external factor maintaining limits to variation whilst permitting different means. Variation clearly is large in all cases and selection in favour of the mean must be weak if it occurs at all. It would therefore appear most likely that selection is not acting on variation per se, except insofar as the paragnaths form part of a larger functional unit in which case selection would act not in favour of particular paragnath numbers but so as to maintain symmetry regardless of the numbers of paragnaths involved. Variation would then be mainly a consequence of the errors inherent in the secretion mechanism, which may be assumed to be comparable in each paragnath group. The significance of variation in group VI is unknown. Its individual pattern distinct from the two functional blocks I-IV and VII-VIII suggests that it may have an entirely separate function or, as some of the results indicate, it may participate in the functions of both blocks. Research on other Nereis species may help to solve this problem. That N. diwersicolor is more variable than the comparatively few other Nereis species that have been investigated is, on the argument presented above, probably due to the diversity of its feeding mechanisms and habitat requirements: carnivorous Nereis with more specialized diets can be expected to experience selection in favour of specific paragnath arrangements. Estuarine animals are frequently variable in their morphology, behaviour and ecology (Remane & Schlieper, 1971) and in several casesan evolutionary or ecological advantage can plausibly be associated with this characteristic, but it is difficult to regard paragnath variation in N. diwersicolor as potentially as adaptive as that, for example, described earlier for the estuarine crab Australoplax (Barnes, 1968). Acknowledgements The authors wish to acknowledge gratefully the provision of the facilities of Dial Cottage

Pamgnath variation in Nereis diversicolor

781

by the Nature Conservancy Council, and of those at the C.E.R.L. Marine Biological Laboratory by Messrs T. E. Langford and J. Coughlan. Mrs Hilary Barnes and Messrs Jack Coughlan and John Phillips very kindly rendered assistance in the field. The facilities of the Cambridge University Computing Service and the numeracy of Dr Roger Moreton were of the utmost assistance; we record our grateful appreciation. References Barnes, R. S. K. 1968 Individual

variation

in osmotic

pressure

of an ocypodid

crab. Comparative

Biochemistry and Physiolom ~7~447-450. Barnes, R. S. K. 1974 E&a&e Biology. Arnold, London. Dales, R. P. 1963 Anneli&. Hutchinson, London. paper for the graphical analysis of polymodal frequency Harding, J. P. 1949 The use of probability distributions. Journal of the Marine Biological Association of the U.K. 28, I&--153. Kaestner, A. 1967 Inuaiebrute zoolo~ Vol. I (Trans. Levi, H. W. & Levi, L. R., eds). Wiley, New York. Muus, B. J. 1967 The fauna of Danish estuaries and lagoons. Meddelelserfru Danmarks Fiskeri- og Havundersegelser (Ny Serie) 5, 1-316. Remane, A. & Schlieper, C. 1971 Biology of brackish water, 2nd ed. (Die BinnengewZsser, Vol. 25). Schweizerbart’sche Verlagsbuchbandlung, Stuttgart. SchBfer, W. 1972 Ecology and Palaeoecology of Ma&e Environments. Oliver & Boyd, Edinburgh. Smith, R. I. 1958 On reproductive pattern as a specific characteristic among nereid polychaetes.

Systematic Zaology 7, 60-73.