Oeeologia (Berl.) 20, 19--32 (1975) �9 by Springer-Verlag 1975

Character Displacement and Coexistence

in Mud Snails (Hydrobiidae)

Tom Fenchel

Department of Ecology, University of Aarhns, /~rhus

Received February 13, 1975

Summary. Populations of coexisting and of allopatrically occurring species of hydrobiid snails (Hydrobia ulvae, H. neglecta, H. ventrosa and Potamopyrgus ]enkinsi) have been studied in 90 localities within three different areas. When H. ventrosa coexists with H. ulvae they show character displacement, i.e., the average body size of the former is smaller and that of the latter is larger. When these species live alone they are of approximately the same size. I t is shown here that the size ratio between the coexisting species usually found (1.3-1.5) allows stable coexistence based on food particle size selectivity alone. Variation in the degree of character displacement from locality to locality is explained by different degrees of genetical isolation of the populations. Coexisting H. ventrosa and H. ulvae have shorter, more well-defined periods of reproduction than they do when they occur alone. H. negIecta is larger than coexisting H. ventrosa and smaller than coexisting H. ulvae. Due to the patchy distribution and the fluctuating populations of this species, and due to the fact that pure H. neglecta po- pulations are rare, data on this species are difficult to interpret. Potamopyrgus ]enkinsi shows a different food particle size selection than the Hydrobia spp. of identical sizes. Competitive interactions between P. ]enkinsi and coexisting Hydrobia spp. are therefore probably weak. In accordance with this, P. ]enkinsi does not show character displacement when coexisting with, e.g., H.ventrosa.

The fact that the major study area, the Limfjord, is only 150 years old as a marine habitat as well as various more recent man-made changes of the coast line allow estimates of the time scale of the mieroevolutionary changes which lead to character displacement.

Introduction

Hydrobf id snails belong to the mos t impor tan t deposit feeding invertebrates

of Nor the rn European estuaries. I n Scandinavian waters four species are found;

Potamopyrgus jenUnsi, and the three Hydrobia spp., H. ventrosa, H. neglecta and

H. ulvae (Muus, 1967). They are all deposit feeders which ingest their substrate

and assimilate the microorganisms a t tached to mineral and detri tal particles

(Fenchel et al., 1975).

The species show different preferences with regard to salinity. Their op t imum

salinity increases in the order P. jenkinsi, H. ventrosa, H. neglecta and H. ulvae.

The species also show differences towards other environmental factors, some of

which are less easy to quantify, i.e., temperature, the degree of water turbulence,

and tolerance to anoxia and desiccation. These differences lead to hab i ta t selections

characteris t ic for each of the 4 species. However, they all show wide and over-

lapping tolerance ranges for these factors. I n the absence of competi t ion each

species would be able to sustain populat ions within the larger par t of the tota l

hab i ta t range in which hydrobi id snails m a y occur (Fenchel, 1975; Muus, 1967).

2*

20 T. Fenchel

Fenche l (op. cit.) showed t h a t the d i s t r ibu t ion of hydrob i ids can only be under-

s tood if no t on ly h a b i t a t selection b u t also compet i t ion , migra t ion and local

popu la t ion f luc tua t ions are t a k e n into considerat ion. Fu r the rmore , i t was shown

t h a t the combina t ion of migra t ion and compet i t ion m a y lead to an a p p a r e n t l y

s table coexistence of two, or somet imes three, of the species in one local i ty . This

is of in teres t since no difference in the w a y the species ut i l ize the i r food resources

have so far been demons t ra t ed .

Popula t ions of Hydrobia spp. are known to be po lymorph ic in the i r shell mor-

phology, p igmen ta t ion p a t t e r n s and isozymes, and the quan t i t a t i ve occurrence

of these forms m a y differ subs t an t i a l ly be tween even closely s i t ua t ed local i t ies

(Lassen, unpubl i shed resul ts ; Muus, 1963, 1967). I n sp i te of migra t ions , therefore,

isolat ion m a y be sufficient to ma in t a in genet ica l differences be tween popu la t ions

wi th in shor t distances.

The purpose of the presen t s t u d y was to inves t iga te whe ther the coexistence

of two species of hydrobi ids , or ig inal ly b rough t abou t t h rough migra t ion or

f luc tua t ing envi ronments , m a y resul t in changes in the popula t ions leading to

resource par t i t ion ing , i.e., " c h a r a c t e r d i s p l a c e m e n t " as def ined b y Brown and

Wilson (1956) and Hu tch in son (1959).

Materials and Methods

Most of the material used was collected in Limfjorden, Northern Jutland. The present study includes collections from 57 shallow water localities in the period May-December 1974. Several of these localities were sampled regularly through the period. The collected material includes about 13000 animals. The sampling localities are described in detail in Fenchel (1975). Additional material was collected outside and in Renders Fjord at the East Coast of Jutland in September, 1974. Twenty-seven localities yielding altogether about 7000 snails were sampled here. Finally, this study includes about 700 animals from the Bothnic Bay at the Tv~rminne area, Finland. These derive from 6 localities ranging in depths from 0.5 to about 4 m. The salinity in the area remains constant at around 5~ The samplings were carried out in

May 1974. Animals were collected in the field by passing sediment through sieves which retain snails

larger than 1.5 ram. Several hundred specimens were usually collected each time. The length of the animals (the distance from the apex to the anterior margin of the

aperture) was measured to the closest 0.25 mm. About 100 specimens were measured in order to quantify the length-frequency distribution of each population.

Data on reproductive periods were in part deduced from comparisons of length-frequency diagrams of the same populations at different times, and in part by counting egg capsules deposited on the shells at different times. The results of these observations are reported elsewhere in more detail (Hylleberg and Fenchel, in preparation) in connection with a study on the growth and lifecycle of hydrobiids.

Food particle size selectivity of the snails was studied in the following way. Animals were allowed to feed on a natural sediment (usually fine, muddy sand from Locality 6) in trays with seawater for 2-12 hrs. A number of specimens of one species (either 2-10 of the same size range, or a representative collection of size ranges from a particular locality) were then rinsed and placed in dishes with filtered seawater. After about 1 hr fecal pellets were collected with a pipette on a microscope slide. With needles the pellets were spread and mixed well and the preparation was sealed with a cover glass. Under the microscope (400 • magnification) the diameter of 200-400 mineral particles were then measured to the closest 2.5 lzm. The relative volumes of the particles were calculated as the third power of the diameter. This technique for measuring food particle size distribution of deposit feeders is

discussed in detail in Fenchel et el. (1975).

Character Displacement and Coexistence in Mud Snails (Hydrobiidae) 21

Results

1. The Coexistence of Hydrobiid Species

The general distribution of hydrobiids in the Limfjord is described in detail in

Fenehcl (1975) and will only be summarized here. H. ulvae is the most widespread

form as it is the only one found in the sediments of the more open areas of the fjord

which have relatively high and constant salinities. I t is also found as the only

species on several stretches along the coast line where there are no particular migra-

tion barriers such as narrow entrances to coves, bays and causeways. H. ulvae is

therefore found as the only representative in many sampling localities. The three

other species are mostly found in coves, bays, and stretches along the coast with a

somewhat lowered salinity. In many places H. ulvae and H. ventrosa form a zone

of overlap along gradients of salinity, typically at the entrance to bays and coves.

Here H. neglecta seems often to have been "squeezed ou t " by competition from

two sides. In some isolated areas (e.g., parts of bays cut off by causeways), a stable

coexistence between H. ulvae and H. ventrosa in a homogenous area is found.

H. neglecta is the least frequent species and is mainly found at salinities of

10-25~ I t usually occurs in more sheltered areas and has a patchy distribution.

I t is also found frequently along "complex" shorelines where the habitats are

subdivided, with pools isolated from the sea at low tide, etc., and where hydrobiid

populations fluctuate due to external factors (freezing in the winter, desiccation

or H~S formation in very hot summer periods). I t is thus a " fugitive" species com-

pared to the other forms. H. neglecta is very rarely found as the only species in a

locality; usually it occurs together with H. ventrosa or H. ulvae, or more rarely

with both.

In localities where the salinities are constantly below about 10~ H. ventrosa

often occurs alone. At salinities below 50/00, it often occurs together with Pota-

mopyrgus ]enlcinsi; at localities where the salinity is constantly below about

l~ the latter is the only species found.

In Randers Fjord only H. ulvae and H. ventrosa are found, the former totally

dominating at the entrance. Going inwards in the fjord, it is replaced by H. ven-

trosa over a distance of about 2.5 km whereafter H. ulvae only constitutes about

5~ of the snails. In the innermost parts of the fjord, P. ]enlcinsi is found.

Outside the entrance of the fjord H. ulvae dominates but in sheltered, vege-

tated patches off the shore it is often found together with H. neglecta.

In the Finnish localities (as well as in the whole Baltic Sea proper), H. negleeta

is absent. In most of the localities, the remaining forms : H. ulvae, H. ventrosa and

P. ]enl~insi coexist.

2. Hydrobia ulvae and H. ventrosa

Typical examples of length-frequency distributions of these two species with

regard to both coexistence and allopatric occurrence are shown on Fig. 1. I t can

be seen that in the ease of coexistence the two species overlap slightly in size

whereas they have nearly identical length-frequency distributions when found

alone.

On Figs. 2 and 3, data from the Limfjord on the sizes of snails for localities

where they coexist (15 localities) and with allopatric occurrence (17 localities) are

22 T.Fenehel

r .l. @

H. ulvae

10

"'" 'i I, I,,, .. / |

i S,ventroso

�9 i

|

2 3 4 5 ~ 7 mm

10

0 2 3 4 5 6 mm

C 2 3 4 5 6 mm

Fig. 1. Length-frequency distributions of the shells of H. ulvae and of H. ventrosa from a locality where they coexist (above) and from two localities where they occur allopatrically

(below). All samples were collected in June 1974

summarized. I t can be seen tha t when living allopatrically both species with a few

exceptions at ta in average lengths between 3 and 3.5 mm. When coexisting,

H. ventrosa is, with two exceptions, smaller than 3 m m and H. ulvae is always

larger than 3.5 mm. As seen from the standard deviations of the length-frequency

distributions, there is very little size overlap for any pair of coexisting populations.

The ratio of lengths between coexisting H. ulvae and H. ventrosa is on average

1.53 and ranges from 1.23 to 1.95 (based on 30 samples collected a t the 15 locali-

ties shown on Fig. 3).

The length-frequency distribution of the snail populations alters somewhat

through the year due to changes in the age structure. However, in coexisting

populations of H. ventrosa and H. ulvae, the ratio between the average lengths

and the small degree of size overlap stays relatively constant through the year,

as exemplified in Fig. 4.

Cgl

e.~ ~ g

~ N

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g ~'g

r162

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24 T. Fenehel

A more thorough study on reproductive periods was only carried out for a

restricted number of stations in the Limfjord. These observations only cover 1974

and there could be considerable variations from year to year. In general, both

species have two peaks of reproduction, one in late spring and one in late summer

or autumn. In a locality where H. ulvae is found alone (Lot. 2), however, repro-

duction was found to occur continuously through the summer from May to August

but at a decreasing rate as can be judged from the numbers of deposited egg cap-

sules. In Locality 6, a fairly isolated cove, where H. ventrosa and H. ulvae coexist

the latter had a peak of reproduction in May and again in August-September

whereas there was no sign of reproduction through the summer. H. ventrosa had

a short period of reproduction in September whereas no eggs or small individuals

( ( 2 mm) were found at all from May to August. In Loc. 9 where the two species

also coexist, H. ulvae reproduced in June - Ju ly with a peak in egg production

around the 1st of July, and H. ventrosa had a well-defined reproductive period in

the beginning of August.

Although sometimes difficult to interpret and many local variations are indi-

cated, length-frequency distributions and scattered observations on the occurrence

of egg capsules from other localities support the general conclusion that when

occurring allopatrically, the snails have a long reproductive period, and when

they are coexisting they have short, well-defined periods of reproduction.

Inside the entrance of Randers Fjord, H. ulvae and H. ventrosa were found

together at all sampling localities. However, at the innermost localities the former,

and at the outermost localities the latter, were often so rare that no quantification

of the length-frequency distributions of these populations could be obtained.

The character displacement is less pronounced than in the Limfjord localities.

The zone of transition, i.e., where both species constitute at least 5 0 of the total

Hydrobia populations, is about 2.5 km. Seven localities were sampled along this

stretch of the fjord. The average ratio of shell lengths (H. ulvae to H. ventrosa)

was only 1.17 (1.13-1.23).

In the Finnish study area one could not expect to find zonation patterns based

on salinity since the area has a fairly constant salinity close to the lower tolerance

limit of both Hydrobia spp. found there. The average length ratio of H. ulvae to

H. ventrosa was found to be 1.32 and ranged from 1.22 to 1.47 in the 5 stations

where both species were found.

3. H ydrobia neglecta

The effect on the length-frequency distribution of H. neglecta populations as

a result of coexistence with other Hydrobia spp. is much more difficult to study

than the mutual effect of H. ventrosa and H. ulvae. First of all, among more than

100 sampling localities in the Limfjord and in Randers Fjord H. neglecta has

nearly always been found together with at least a smaller population of one or

both of the other species (Fenchel, 1975). I t is therefore not possible to compare

allopatrieally occurring populations of H. neglecta with populations coexisting

with the other species. Secondly, as already pointed out, H. neglecta often occurs

in patches in localities with fluctuating populations of hydrobiids; it is therefore

difficult to find criteria for choosing localities where it can be considered to live

in stable coexistence with the other forms.

Character Displacement and Coexistence in Mud Snails (ttydrobiidae) 25

6[~ 42 21 7oF 72 17 7oc ~s G~

i tli, �9 la,' 'I 'I

Fig. 5. Average lengths of H. ulvae, of H. neglecta (crosses) and of H. ventrosa on 3 localities where all three species coexist and on 5 localities where only the two latter species are found.

All samples are from the summer of 1974. Legends as for Fig. 2

In the Limfjord, H. neglecta is practically always found together with H. ven-

trosa; H. ulvae is also found in a number of localities. In Fig. 5, a number of

localities where the composition of the hydrobiid populations remained fairly

constant troughout the summer of 1974 is shown. I t can be seen that the average

length of H. neglecta is greater than that of coexisting H. ventrosa and smaller

than that of H. ulvae. The length ratio of H. negtecta to H. ventrosa was found to

be 1.13 on an average (1.06-1.22) when these two species were found alone, and

1.08 (0.95-1.18) when H. ulvae is present too. The average length ratio of H. ulvae

to H. neglecta was found to be 1.42 (1.18-1.55).

Outside Randers Fjord, 13 localities in which H. ulvae was found together

with H. neglecta were sampled. The average length ratio was 1.20 (1.09-1.38). In

these localities, the average lengths of both species were lower than those found

in the Limfjord localities.

4. Potamopyrgus jenkinsi

This species was found to coexist with H. ventrosa in several localities in the

Limfjord with low salinities as well as together with both H. ventrosa and H. ulvae

in the Finnish localities. No indication of any systematic size ratio to the coexist-

ing hydrobiids nor any systematic difference from populations living in the

absence of Hydrobia spp. could be found. In the Finnish localities, its size distri-

bution nearly totally overlapped with that of H. ventrosa. This is probably only

the case in the spring since much larger, empty Potamopyrgus shells from the

previous summer were found in some of the localities.

26 T. Fenehcl

200

I00

50

20

..," / o, A , "

+ ]

+ + I 0

. / ~ o," �9

�9

A P, j enk ;ns ;

�9 H.vent rosa H. negtectcl

O H. u tvee

I I I I I

i[+

60

40

20

0

60

40

20

z,0

20

she l l Length (turn) l I I I l l I I I

2 3 z, 5 6 ? 8 9 1 0 4

0

, I I I

|

�9 i t ~ i t

16 32 1 8 256 512

6 7

Fig. 6. Median diameter of ingested food particles of the 4 species of hydrobiids plotted against shell length

Fig. 7. Food particle size distributions (volume ~ ) for the populations of H. ulvae (open circles) and of H.ventrosa (filled circles) from a locality where the species coexist and from

two localities where they live alone

5. Food Particle Size as Function of Body Length

In Fig. 6 the median food particle size is plotted against shell length. I t can

be seen tha t the three Hydrobia spp. show the same relationship between particle

size and body length. The slope of the calculated regression line is not significantly

different from 1, i.e., the relation can be considered as linear. I t can also be seen

tha t the preferred food particle size of Potamopyrgus is about 3 times higher than

tha t of Hydrobia spp. of identical body sizes.

In Fig. 7 the food particle size distribution of representative collections of

H. ventrosa and H. ulvae from localities where they coexist and where they are

found allopatrically are shown.

Character Displacemen$ and Coexistence in Mud Snails (Hydrobiidae) 27

Discussion

1. The Concept of Character Displacement

Brown and Wilson (1956) coined the term "character displacement" to de-

scribe the phenomenon that where two closely related species coexist they may

differ more from each other than when each of the species are found alone.

Two mechanisms may lead to character displacement. In a zone where popula-

tions of two closely related, interfertile forms overlap, characters may develop

which hinder interbreeding. This will happen if the mixed offspring has a lower

fitness than either of the parental forms. Character displacement may also develop

in conjunction with a relaxation of interspeeifie competition where two not inter-

breeding species overlap geographically. Clearly, where two species coexist indi-

viduals of either will be more fit than others if they can utilize resources not

exploited by individuals of the other species. The degree of character displacement

will be balanced by on one side the intensity of interspecific competition and on the

other side the availability of resources outside its normal preference range. The

latter limit may be set by competition with a third species, by rari ty of such

resources or by physiological and morphological properties of the species itself

which can only be changed slowly in the evolutionary process.

The stable coexistence may be brought about by a differential utilization of

resource qualities or by utilizing the same resources in different time periods

(e.g., seasons).

Let us consider competing species which have only one type of limiting resource

the different qualities of which can be pictured as a one-dimensional axis (e.g., food particle size) and that the utilization functions of the species are normal

curves (c/. Fig. 7). In this case theoretical work (MacArthur, 1972; May, 1973)

shows that stable coexistence is possible only if the distances between the modes

of the utilization functions are somewhat larger than their standard deviations.

MacArthur (op. cir.) also brings several examples from field populations of coexist-

Lug congeners which illustrate the predictions of the theoretical work.

Hutchinson (1959) reviewed the then known cases of character displacement.

These eases nearly all imply size differences of whole animals or of some trophic

organs, mostly bill dimensions of birds. I t was empirically found that length ratios

of about 1.3 (weight ratios of about 2) permit coexistence of congeners. Further

examples and references may be found in MacArthur (1972) and Sch0ener (1965).

When interpreting size differences in coexisting congeners, it is implied that they

lead to resource partitioning according to food particle or prey size. This has been

documented for some cases by Hespenheide (1973).

The reason why most documented cases of character displacement involves

dimensional and temporal characters rather than other adaptive features is prob-

ably in pa r t due to the fact the former are easy to detect and quantify. Further-

more, body size is probably quickly changed by selection (c]. domestic animals).

Robertson and Reeve (1952) after 15 generations of selection in populations of

Drosophila, produced divergent lines differing about 25% of the initial size.

Finally, the effect of competition of related species brought together within the

same area will in most cases lead to habitat specialization rather than to resource

partitioning within one habitat (MacArthur, 1972).

28 T. Fenchel

When interpreting the present findings on hydrobiid snails, a number of

aspects will have to be discussed.

2. Factors Influencing the Size of ttydrobiids

I t is clear that a number of environmental factors or genetical differences may

influence the size of the animals independently of interspecifie competition.

Factors determining the sizes attained by H. ulvae from different populations

have been treated by several authors (Fish and Fish, 1974; Muus, 1967 and refer-

ences therein). Fish and Fish (op. cir.) stress the substrate as an important factor;

they found larger specimens of H. ulvae in muddy than in sandy habitats and at-

tr ibuted this to a higher growth rate in the former type of sediment. During the

present study, the sediment was analysed mechanically for all sampling localities.

The observation of Fish and Fish could in general be confirmed, i.e., animals from

sandy bottoms are usually somewhat smaller than from silty ones. Thus, for

example, the sampling localities 57 and 58 have relatively clean and coarse sandy

sediment (Fig. 3). At very low salinities ( < 50/00) very small individuals of H. ven-

trosa are often found. Finally, variation in average shell size between different,

allopatrically occurring snails which could not be correlated with any environ-

mental factor is often found. They probably reflect genetical differences between

the populations similar to the variations in pigmentation and in the shell type

which are not yet understood.

However, Figs. 2 and 3 show altogether 32 sampling localities and each of the

groups of localities (H. ventrosa and H. ulvae coexisting, H. ulvae living alone and

H. ventrosa living alone) represent a wide variation in environmental factors

(sediment, salinity, turbulence, presence or absence of macrophytes). I t can be

seen that the effect of the presence or absence of a competing congener overrides

all other factors in determining the size of the animals.

3. Interpretation of the Differences in Sizes and in Lifecycles

in Terms of Resource Partitioning and Coexistence

The width of the resource utilization function (i.e., "niche width" in the sense

of, e.g., Levins, 1968) will be for any population a function of (I) the variance of

the resource qualities consumed by an individual and (2) the variation among

individuals due to environmental and genotypieal variation and age structure.

If these can be quantified, and if we can assume a single resource dimension, as

previously discussed, we can estimate the size difference between individuals of

two species of Hydrobia required for their stable coexistence. We know that

there is a linear relation between the modal particle size consumed and shell

length (Fig. 6). Fig. 8 shows the length frequency distribution of two Hydrobia

populations as well as the size frequency distributions of food particles consumed

by some size groups of snails plotted on probability paper. I t can be seen that the

standard deviation of the length distribution of natural snail populations is about

0.i log S units and that of the food particle sizes about 0.4 log S units. The relation

between length and food particle size is linear. Thus, in order to have the resource

utilization curves spaced more than 1 standard deviation, the ratio in average

Character Displacement and Coexistence in Mud Snails (Hydrobiidae) 29

99.5

99

95

90

80

7O

6O

5O

40

30 ~

2O

10

5

1

0,5

. :E "/0

/ /

, J

oZ o l i e / /

..... / o/ / ,,/ /---:/

/ 0

/

o_J

she l l l eng th ( log 2 ram} i t i ~ , i , , , i .

1 2 3 3

OH.u lvae

xH . neg lec t a

�9 H. ven t rosa

;n~es ted pa r t ; t i e d;.am.(IocJ 2 .urn) t , ,

4 5 6 7

Fig. 8. Shell length distributions of two populations of Hydrobia spp. floe. 10, July) and size distributions of loartieles ingested by single size groups of hydrobiids. :Both distributions are

plotted eummulatively on probability paper with a log2 scale as horizontal axis

9 "5

)5

~0

8O

70

50

50

40

]0

20

10

5

shell lengths of the populations would have to be (0.4 + 0.1) log 2 units or a factor

of about 1.4.

These calculations are of course very crude since neither of the frequency

distributions are in fact perfectly log-normal. In the case of length distribution

the calculated standard deviations may indicate an overestimate of overlap and

therefore of the required size ratios. Nevertheless it is seen that such simple con-

siderations may lead to values comparable to those found by Hutchinson (1959)

and those found during the present investigation. The actual degree of resource

overlap with regards to food particle size for coexisting H. ventrosa and H. ulvae

is shown on Fig. 7.

The average size ratio for coexisting H. ventrosa and H. ulvae in the Limfjord

localities was found to be 1.53. This probably allows for coexistence based on

food particle size selection alone. There is, however, a considerable variation in

the length ratios (1.23-1.95) from locality to locality. This is even more clear when

the l~anders Fjord localities, where the average ratio was lower, are taken into

consideration. Such a variation could be expected. The coexistence of hydrobiid

species is probably initially always brought about by migration pressure (Fenchel,

1975) and any local genetical changes will be a balance between gene flow from

outside the zone of overlap and local selection pressure. Most of the localities

studied in the Limf]ord where H. ventroscb and H. ulvae coexist are relatively

isolated by exposed beaches (which are not inhabited by hydrobiids), causeways

30 T. Fenchel

or narrow entrances to bays and coves, but a non-quantifiable variation of course

exists. In Randers Fjord, there are hardly any geographic barriers along the

stretch studied and it is not unlikely that a pure H. ulvae population may be

found in the deeper, more saline middle parts of the fjord extending much further

inwards than the shore. This was not investigated. Under all circumstances it is

likely that migration, and therefore gene flow, may occur at a higher rate in this

fjord, counteracting local microevolution.

The Finnish populations of H. ulvae and H. ventrosa showed an average ratio

of 1.32. This is somewhat lower than the average ratio for the Limfjord localities

but within the expected range according to the considerations given above. With

regards to the Finnish hydrobiids, it should be pointed out tha t these snails show

habitat expansion relative to the Danish localities. This is due to the absence of a

number of competing species (littorinids, rissoids) which are not able to live in the

brackish Bothnian Sea. Thus they are also found on submerged macrophytes and

on hard substrates in this area. I t cannot be ruled out tha t some, insufficiently

studied microhabitat differences between the two species also facilitate their

coexistence in this area.

The differences in reproductive periods between allopatrically living and

coexisting populations of H. ulvae and H. ventrosa could not be interpreted in

detail. Hutchinson (1959) found that in forms which coexist on the basis of size

difference, the largest form always reproduce before the smaller one so that the

largest one remains so throughout the lifecycle. These observations were based on

annual insects (corixids). H. ulvae and probably also the other species, may attain

an age of 1.5-2 years (Fish and Fish, 1974) and the observation of Hutchinson

would not necessarily be valid in this case but somewhat more complex conditions

could be expected. A detailed analysis will require much more precise data on

lifecyeles from different localities than are available. I t can only be stated that

coexistence seems to limit the reproductive periods of the populations.

The fact tha t H. neglecta does show a relatively constant size ratio to coexist-

ing H. ulvae and H. ventrosa will lead to resource partitioning with regards to

food particle size. However, according to the considerations given above the size

ratio to coexisting H. ventrosa is not large enough to explain coexistence on the

basis of this alone. As discussed earlier (see also Fenchel, 1975), H. neglecta usually

shows a patchy distribution and fluctuating population sizes. I t is probably

competitively superior to other hydrobiids under more extreme conditions and

in sheltered, vegetated areas with salinities of 15-25~ This explains its presence

in the area but it does not explain why when it is found together with H. ventrosa

the size ratio is relatively small. I t is possible tha t the distribution pattern of

H. neglecta does not favour the sufficient gentical isolation. I t is also possible

tha t there are more subtle, hitherto unobserved differences between the resource

utilization of H. ventrosa and H. neglecta which do not imply food particle size

selectivity. Work in progress (Hylleberg, unpublished observations) indicates

that there are differences in digestive enzymes of the two species.

Finally with regards to Potamopyrgus ]enl~insi, Fig. 6 clearly shows that it

will under any circumstances only compete slightly with the Hydrobia spp. for

food particles. Various, presumably morphoIogical, differences in this different

genus already ensures a resource selectivity different from that of the Hydrobia

Character Displacement and Coexistence in Mud Snails (Hydrobiidae) 31

spp., at least in adult specimens. We would not expect, nor do we find, character

displacement when P. jenkinsi coexists with H. ventrosa or H. ulvae.

4. The Time Scale Involved in the Evolution

of Character Displacement in H. ulvae and H. ventrosa

The study of the distribution and evolution of character displacement of

hydrobiids is of special interest in the Limfjord since the presence of these animals

as well as tha t of the entire marine fauna, is relatively recent. In the present post-

glacial period, the natural state of the fjord is closed where the entrance to the

North Sea is now found. Before the beginning of last century the fjord was only

open at its eastern end and the western and central parts were actually a number

of large, interconnected freshwater lakes. In 1825, following a storm, the western

entrance broke open and it has since been kept open artificially for navigational

purposes and due to fishery interests. After the opening of the western entrance,

the western parts became marine ( ~ 300/00) and in the open parts of the remaining

fjord the salinities range from 20 to 300/00. In the years following the opening,

a marine fauna invaded the fjord. This was studied by naturalists in the last

century (Collin, 1887) and the present distribution of hydrobiids (with the ex-

ception of Potamopyrgus jenkinsi which first came to Denmark in this century;

see Bondesen and Kaiser, 1949) derive from this period. I t is not known how fast

the present distribution patterns developed [unfortunately Collin (1887) did not

distinguish between the different species of Hydrobia]. Under all circumstances,

it can be concluded that the evolution of character displacement in the different

localities with coexistence has taken place within less than 150 years, i.e., less

than 150 Hydrobia-generations. I t is certain that the patterns of distribution of the

snails have altered more recently in some areas due to man made changes (con-

struction of causeways and channels, land reclamation projects) and in some

cases it can be concluded that character displacement evolved within a much

shorter time scale. Locality 6 consists of the opening of a now abandoned channel

which was buildt in the years following 1850 but is now nearly isolated from the

open fjord except at very high tides. Here, the evolution of populations of very

large sized H. ulvae and very small sized H. ventrosa must have taken place

within at most 120 years. Some localities indicate tha t the evolution of character

displacement may take place much faster. Locality 23A is a small area isolated

by a causeway built in the sixties of this century from a larger Bay (Skive Fjord).

Outside the causeway, H. ulvae is the only species found, but behind the causeway

a population of H. ventrosa is found coexisting with H. ulvae. H. ventrosa probably

first attained populations there after the construction of the causeway being

protected from a strong migration pressure of H. ulvae from the open bay. This

locality indicates character displacement, i.e. the individuals of H. ulvae inside

the causeway are larger than those found immediately outside (Locality 23, el.

Figs. 2 and 3) although the environmental conditions do not seem to differ signifi-

cantly between the two sides of the causeway.

5. Future Investigations

The present s tudy a s well a s the study of Fenchel (1975) show the significance

of biotic interactions; competition and migration in conjunction with habitat

32 T. Fenchel

selection and env i ronmenta l complex i ty for unde r s t and ing the d i s t r ibu t ion

p a t t e r n s of hyd rob i id snails. The p resen t s t u d y fur ther shows the nescess i ty of

popu la t ion genet ical considera t ions for a comple te analys is of the found pa t t e rn s ;

i.e., a quan t i f i ca t ion of select ion pressures in and gene flow be tween the m a n y

subpopula t ions of the snails.

Acknowledgements. Parts of these studies were supported by grants from "Statens Natur- videnskabelige Forskningsrs My sincere gratitude is due to Dr. Annikki Lappalainen for collecting hydrobiids in the Finnish localities. I am grateful to Drs. Freddy B. Christianson, Jorgcn Hylleberg and Hans H. Lassen for discussions; the latter also collected parts of the material in the Limfjord and in Randers Fjord. Above all my gratitude is due to Ms. Elsebeth Glob who carried out the greater parts of the samplings as well as the measurements on the collected material.

References

Bondesen, P., Kaiser, E. W.: Hydrobia (Potamopyrgus) jenkins~ Smith in Denmark, illustrated by its ecology. Oikos 1, 252-281 (1949)

Brown, J., Wilson, E. 0.: Character displacement. Syst. Zool. 5, 49-64 (1956) Collin, J . : Om Limfjordens tidligere og nuvmrende marine Fauna reed smrligt Hensyn

til Bl~ddyffaunaen, 168 pp. Copenhagen: Gyldendalske Boghandels Forlag 1887 Fenchel, T.: Factors determining the distribution patterns of mud snails (Hydrobiidae).

Oecologia (Berl.) 20, 1-17 (1975) Fenchel, T., Kofoed, L. H., Lappalainen, A.: Particle size selection of two deposit feeders:

the amphipod Corophium volutator and the prosobranch Hydrobia ulvae. Mar. Biol. (in press, 1975)

Fish, J .D. , Fish, S.: The breeding cycle and growth of Hydrobia ulvae in the Dovey Estuary. J. mar. biol. Ass. U.K. 54, 685-697 (1974)

Hespenheide, H. A. : Ecological inferences from morphological data. Ann. Rev. Ecol. Syst. 4, 213-229 (1973)

Hutchinson, G. E. : Homage to Santa Rosalia or why are there so many kinds of animals ? Amer. Naturalist 93, 145-159 (1959)

Hylleberg, J., Fenchel, T.: The growth and lifecycle of mud snails (Hydrobiidae). In preparation

Levins, R.: Evolution in changing environments, 120 pp. Princeton: Princeton University Press 1968

]KacArthur, R. H.: Geographical ecology, 269 pp. New York: Harper and Row 1972 May, R. IV[.: Stability and complexity in model ecosystems, 235 pp. Princeton: Princeton

University Press 1973 Muus, B. J . : Some Danish Hydrobiidae with the description of a new species, Hydrobia

neglecta. Proc. iKalacol. Soc. Lond. 35, 131-138 (1963) Muus, B. J. : The fauna of Danish estuaries and lagoons. Medd. Danm. Fisk. Havunders.,

N.S. 5 (1), 1-316 (1967) Robertson, F. W., Reeve, E.: Studies in quantitative inheritance. I. The effects of selection

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Dr. Tom Fenchel Department of Ecology University of Aarhus DK-8000 i~rhus C, Denmark