Mammal Rew. 1985, Volume 15, No. 1, 13-21. Printed in Great Britain

The feeding ecology of the European Water shrew SARA CHURCHFIELD

Department of Biological Sciences, Chelsea College, University of London, Hortensia Road, London S WlO OQR

ABSTRACT This review examines our knowledge of the feeding ecology of the European Water shrew, Neomys fodiens. It describes and discusses the different methods which have been used to study the diets of Water shrews, from the first casual observations to the discovery of food caches and food remains in the wild, and the analysis of stomach con- tents and faecal pellets of trapped animals. These studies have revealed that Water shrews feed on a variety of invertebrate and vertebrate prey from tiny freshwater dip- teran larvae to sizable fish and frogs. Although aquatic prey are seen to be the major dietary component in most studies, terrestrial prey are also important and may be eaten in an equal proportion. Laboratory studies have increased our knowledge of the foraging behaviour of Water shrews but there is still much to be learnt, especially about underwater prey location.

INTRODUCTION Three species of shrew, the Water shrew (Neomysfodiens), the Common shrew (Sorex araneus) and the Pygmy shrew (S. minutus), are sympatric over most of their range in Europe and mainland Britain. Of these, the Water shrew is the largest and has the ability to exploit both terrestrial and aquatic environments for food. With these attri- butes Water shrews might be expected to be both widespread and numerous. Instead, they are extremely elusive, especially in Britain where they appear to have small and localized populations (Shillito, 1963; Churchfield, 1984b) making them a difficult species to study in the field. Consequently, the ecology of Water shrews is poorly understood and information about their feeding habits is particularly scanty. For example, there has been little study of the feeding habits of wild Water shrews on a continuous basis throughout the year in order to discover what proportions of the diet are aquatic or terrestrial in origin, and whether there are seasonal differences in the mode of foraging. More information about their dietary requirements might indicate why Water shrews are not more common.

This paper reviews our knowledge of the feeding ecology of the Europew. Water shrew gleaned from field and laboratory studies, and indicates further avenues for research.

FIELD STUDIES Few people have reported observations of Water shrews feeding in their natural habitat apart from Sawyer (1946) who watched a shrew catch tadpoles and a stone loach in a stream, and Brewster (1966) who witnessed the capture of a water snail.

The first detailed study of the predatory habits of wild Water shrews arose from the observation of four food caches beside a drainage ditch in Poland (Buchalczyk & Pucek, 1963). These caches consisted of up to 106 partially-eaten frogs (Rana

14 S. Churchfield

temporaria and R. arvalis), two fish (Esox lucius and Lota lota), over 600 freshwater snail shells (mostly of Radix ovatu, Lymnaea stagnalis and Planorbarius cottleus), and a few remains of water beetles (Dytiscus sp.). It was not known, however, how many shrews were involved in this food caching, and observations were restricted to October and November.

It .was Wolk (1976) who first provided an indication of the range of prey taken by Water shrews. He found Water shrews inhabiting a series of drainage ditches and underground pipes interspersed with wells in which freshwater animals accumulated. He observed that the shrews left the remains of their prey on flat surfaces such as pieces of wood afloat in the wells. So, he provided wooden rafts in the wells for the shrews to feed on and which facilitated his recovery of any remains. The rafts were inspected during two successive autumns and winters. The wide range of prey found is summarized in Table 1. All the prey were of aquatic origin. Most important were insects (particularly trichopterans), gastropods and frogs, but fish were also eaten. The

Table 1 Percentage composition of the autumn and winter food items of N. fodiens found by Wotk ( 1 976) ajter an analysis of remains of

940 prey animals collected from food rafts

Autumn Winter

Insects Anabolia sp. Limnephilus sp. Molanna sp. Notidobia sp. Trichoptera indet. Dytiscus sp. Nepa sp.

Anisus sp. Anodonta sp. Bathyomphalus contortus Bithynia tentaculata Galbo contur G. truncatula Lymnoea stagnalis Pisidium sp. Pknorbarius corneus Planorbis planorbis Radix peregra Segmentina nitida Viuiparus contectus

Amphibians Rana temporaria Bujo bufo

Gasterosteus aculeatus

Sorex araneus

Molluscs

Fish

Mammals

(13.2) (55.4) 0 0.4 0 38.0 3.3 1.1 0.7 6.5 0 2.5 0.7 0.9 8.6 6.0

(72.2) (22.2) 0 0.1 0 0-6 0 0.1 0 1.5 1.3 4-1 0 0.1 0 0.3 0 0.3 4.0 1.3 0.7 0.1 58.3 1.1

0.7 0.1 1.2 0.6

(14.6) (20.3) 14.6 20.2 0 0-1

0 2.0

0 0.1

Food of Water shrews 15

diet changed slightly as winter progressed; the percentage composition of gastropods decreased while insects and amphibians increased, and there was a general increase in diversity of prey taken. Again the number of shrews involved was unknown but Wolk estimated that two to four animals used the rafts.

Kraft & Pleyer (1978) also used the technique of analysing food remains when studying the diet of Water shrews living around 12 fish ponds in West Germany. They found that fish (mainly tench, Tinca tinca), aquatic gastropods and insects (mostly trichopteran larvae) were the major prey items. When fish and insects were in short supply, gastropods were taken in greater proportions.

Other workers have used stomach analysis as a method for studying the diet of wild Water shrews; Niethammer (1978) studied the summer diets of 45 N. fodiens and 18 N. anomalus living along a brook in the Austrian Alps. Aquatic prey predominated in the diets of both shrews, but some terrestrial items were taken. In contrast to the findings of Buchalczyk & Pucek (1963) and Woik (1976), all the prey taken were invertebrate (Table 2) and comprised mainly aquatic larvae of insect such as tri- chopterans, plecopterans and dipterans together with some insect imagines, amphipods and, occasionally, opilionids and lumbricids. Approximately 767, of prey were aquatic. Illing, Illing & Kraft (1981) found remains of aquatic gastropods and small fishes as well as aquatic insects and their larvae in the stomachs of two N. fodiens in a similar habitat. They observed that shrews also preyed upon terrestrial animals, though aquatic foraging was apparently more successful than terrestrial foraging.

Table 2 Diet of 45 N. fodiens revealed by stomach

analysis (After Niethammer, 1978)

Prey item composition

Insect larvae Plecop tera Ephemeroptera Diptera

Simuliidae Psy chodidae Chironomidae Dixidae Limoniidae

Trichoptera Odonata Amphipoda

Insect imagines Ephemeroptera Diptera Coleoptera Neuropt era Indet.

Opiliones

Lumbricidae

Soricidae

15.0 16.5

18.1 1.6 2.4 0.8 3.9

16.5 0.8 0.8

0.8 3.9 0.8 0.8 13.4 1.6

1.6

0.8

16 S. Churchfield

Stomach analysis may give a more complete picture of the feeding habits of known numbers of individuals than analysing food caches or remains, but it is a wasteful pro- cess entailing large-scale mortality in order to obtain the necessary number of samples. For a species such as N . fodiens, which has rather small and localized populations, this procedure could be devastating. An alternative approach is faecal analysis which has

Table 3 The percentagefrequency of occurrence of prey items in the diet of N. fodiens inhabiting water-cress

beds (Af ter Churchfield, 1 9 8 4 ~ ) ~~~~ ~ ~

Spring Summer Autumn Winter

Number of samples Terrestrial prey

Carabids Staph ylinids Chrysomelids Coleopteran adults indet. Coleopteran larvae Hemipteran adults Dipteran adults Tipulid larvae Other dipteran larvae Lepidopteran larvae Hymenopterans Dermapterans Formicids Collembolans Acarines Araneids Opilionids Isopods Geophilomorphs Lithobiomorphs Diplopods Gastropods Lumbricids

Coleopteran adults Coleopteran larvae Hemipteran adults Trichopteran adults Trichopteran larvae (cased) Trichopteran larvae (uncased) Plecopteran larvae Ephemeropteran larvae Simulium sp. larvae Other dipteran larvae Asellus Gammarus Gastropods Ostracods Osteichthyes

Aquatic prey

32

11.0 13.8 0

10.5 12.5 2.6

49.2 0 1.3 5.0 0 0 5-0 0

11.3 124 0

15.7 18.3 1.3 1.3

29.3 21.0

4.0 0 0 5.0

73.9 1.3

18.8 4.2 5.0

10.8 80.4 13.4 0

12.5 0

48

10.2 13.5 8.5

19.1 0

17.0 59.2 2.9

18.6 1.8 0 1.8

18-2 0

16.0 15.4 13.6 15.5 5.0 0

13.3 14.2 10.5

2.9 0 4.2 0

22.5 3.6

17.1 0

10.1 28.6 70.1 33.4 0

10.7 0

40

2.1 14.6 0

20.9 8-3 0

56.3 0 0 2.1 0 0 6-3 4.2

12.5 6.3 2.1 8.3 6.3 2.1 4.2

25.0 27.1

2.2 0 0 4.2

39.6 6.3

41.7 0

20.8 29.2 62.5 31.3 2.1

12.5 4.2

41

3.3 2.2 0

18.3 2.1 7.7

54.0 7.7

12.9 3.3 3.3 0 0 0 8.6

15.2 2.2 4.4 7.7 2.1 6.3

26.1 28.3

2.2 2.2 0 0

17.7 4.2 3.3 4.3 0

20.0 78.3 19.9 0 5.4 0

Food of Water shrews 17

largely been overlooked in the study of small mammal diets. Remains of most prey types can be found in the faecal pellets of shrews; not only the non-digestible chitinous components but also the softer parts such as the body wall of lepidopteran larvae which have escaped digestion are found. Criticisms of the technique are discussed in Churchfield (1982). Faecal analysis has the overriding advantage of producing numerous, random samples from a population without killing individuals and thus can give a continuous record of diet during individuals’ life-times.

I t was Churchfield (1979) who first used faecal analysis of live-trapped Water shrews as a means of investigating their feeding habits. The diets of shrews caught in two different habitats (water-cress beds and deciduous woodland) comprised only invertebrate prey. In the woodland, only terrestrial prey such as insects, isopods, myriapods and lumbricids were taken. At the water-cress beds, these were augmented by aquatic crustaceans, trichopteran and dipteran larvae. But sample numbers were small and few months were covered.

A much more extensive study of the seasonal diets of wild Water shrews inhabiting water-cress beds in southern England was made by Churchfield (1984a) using the faecal analysis technique. Water shrews were captured with Longworth live-traps over a 2-year period and the faecal pellets produced by each individual in a trap were collected and analysed for prey remains.

The prey items found in different seasons in this study are summarized in Table 3. Although a wide range of terrestrial and aquatic prey were taken in all seasons, some

-

>. W

2 3 9 a

a a

c ln W

W I-

- >- W a a 2 t

Adull Coreopterais

Adult Hemipterons

Insect Lorvoe

lsopods

Myrio pods

Aroneids 8 Opilionids

Gastropods

Lumbr k i d s

Tnchopteran Lorvoe

Dipteran Larvae

Other Insect Larvae

0 I 0 20 30 % Composition

Fig. 1. The percentage composition of major prey types in the diet of N . fodiens revealed by an analysis of 161 faecal samples. (After Churchfield, 1984a).

18 S. Churchfield

items such as dermapterans and hymenopterans occurred very infrequently. Only a single occurrence of vertebrate remains was recorded, from a fish. There was no signi- ficant difference in the diversity of prey taken between winter (November-March) and summer. The size of prey taken ranged from the larger tipulid and trichopteran larvae of > 40 mm to the very small Simulium sp. larvae, chironomid larvae, mites and ostra- cods of < 4 mm, although the extremely small size of the latter cannot preclude the possibility of accidental ingestion. Remains of frogs were never found, unlike the studies of Buchalczyk & Pucek (1963) and Wolk (1976) in which they appeared to be major dietary items, but this may have been due to differences in their availability.

Churchfield (1984a) found that shrews foraged underwater throughout the year and 33-670); of prey were of aquatic origin, with a mean of 50% for the whole sampling programme. The dominant item in the diet in all months was Asellus sp., closely followed by cased trichopteran larvae. Other important items in most months were Gammarus sp. and aquatic dipteran larvae including chironomids and the small Simulium sp. From terrestrial sources, adult coleopterans (primarily carabids and staphylinids), adult dipterans (mainly muscids) and gastropods occurred in major proportions. Despite the occasional abundance of emerged adults of insects such as trichopterans and ephemeropterans, these were rarely eaten. The overall composition of major prey types in the diet are shown in Fig. 1 which demonstrates the importance of aquatic prey, particularly crustaceans.

LABORATORY STUDIES WITH CAPTIVE SHREWS Our knowledge of the feeding habits of Water shrews has been augmented by a few records describing how they may be maintained in captivity and commenting on their behaviour (Kelway, 1945; Crowcroft, 1955; Hawkins & Jewell, 1962). Lorenz (1952) fed Water shrews on small fish and frogs while Cranbrook (1959) sustained his shrews mainly on earthworms, slugs and snails of which the former were the most preferred. Small fish (sticklebacks and tench) and aquatic gastropods, crustaceans and insects were also readily taken when offered in a tank of water. The food trials conducted by Churchfield (1984a) revealed that captive shrews would even catch and eat aquatic hirudineans and small turbellarians, though crustaceans such as Gammarus and Asellus were preferred. Aquatic gastropods, though often caught, were rarely eaten in this study.

Tupikova (1949) suggests that Water shrews prefer prey of aquatic rather than terrestrial origin, but the relative success of each method of foraging has not been investigated. The efficiency of underwater prey location was, however, investigated by Churchfield & White (unpublished) using a glass tank (75 cm x 30 cm) filled to a depth of 10 cm with water in which were placed eight individuals of one of the following prey types: (1) live, active Calliphora larvae ( 2 ) freshly killed, inactive CalZiphora larvae and ( 3 ) dummy Calliphora larvae made from white tissue paper tied up with cotton, resembling the size and shape of larvae. A Water shrew which had been starved for 1 h was placed on a rock in the tank and its foraging activities observed and recorded for 30 min. Each prey type was tested separately using three different shrews with two trials/shrew.

Water shrews were excellent at retrieving prey underwater and were able to locate active and inactive prey with equal ease, as shown in Table 4, but they were unable to distinguish between real prey and cylindrical objects resembling prey; this is indicated by the high rate of retrieval of dummy prey. Each dummy prey was only discarded when it had been taken out on land and bitten several times. Prey location appeared to

Food of Water shrews 19

Table 4 Prey lofation by N. fodiens in laborotory trials

Mean 9 , of each prey type caught trials

Number of

Live Calliphora larvae Dead Calliphora larvae Dummy Calliphora larvae

92 6 88 6 94 6

be by direct snout contact-removing the vibrissae, for example, did not impair prey location.

The exploratory/foraging dives made by the shrews had a maximum length of only 4 s. Shrews would dive to depths of 75 an or more in larger tanks, but the duration of each dive was still only 4 s.

Clearly, there is much more to be learnt about the foraging behaviour of Water shrews, and research is continuing in this field.

DISCUSSION The studies reported in this review reveal that Water shrews are opportunist feeders which take a great variety of aquatic and terrestrial prey. The size of prey items taken covers a wide range, from the small aquatic dipteran larvae up to the much larger fish and frogs. How these larger prey are caught and how frequently they are taken in the presence of smaller and more manageable invertebrate prey is unknown. The studies of Buchalczyk & Pucek (1963) and Waik (1976) suggest that frogs are common dietary items, at least of Polish Water shrews. There is only one known incident of a wild Water shrew in Britain eating amphibian prey, an adult smooth newt (Triturus vulgaris); this was reported by Pernetta (1976).

It is clear from all these studies that Water shrews forage underwater throughout the year and that aquatic prey are a major component of the diet; the shrews studied by Buchalczyk & Pucek (1963), Wofk (1 976) and Kraft & Pleyer (1978) apparently took only aquatic prey. Only in Churchfield’s study (1984a) did aquatic prey constitute as little as 33-67?,,, the rest comprising a wide range of terrestrial invertebrates. This may have been due to the differences in availability of certain prey types in the habitats under study. Alternatively, it could reflect the method of study; diet analyses based upon food caches and uneaten prey remains left on land may not reveal the full range of prey taken because they are likely to be biased towards the larger items which are most easily found and identified and which are most resistant to loss through decay or dispersal. It is interesting to note that, according to Hamilton (1930), the bulk of the diet of the American Water shrew (Sorex palustris) comprises terrestrial insects including hemipterans, coleopterans and dipterans. Aquatic invertebrates such as plecopteran nymphs and turbellarians were taken less frequently. Only 500,b of stomachs of this shrew examined by Conaway (1952) contained aquatic prey.

The ability to forage underwater enables Water shrews to reduce competition with other more terrestrial species, but their tendency towards terrestrial foraging leads to considerable dietary overlap with other shrews; overlap between N. fodiens and S. araneus, its major potential competitor, was 449, according to Churchfield (1984a).

20 S. Churchfield

Considering the abundance and accessibility of aquatic prey, it is curious that Water shrews do not forage entirely in the water, but the ease with which prey can be caught may be an important factor. Foraging/exploratory dives by captive shrews are very short and, though prey retrieval is good, it is apparently inefficient because inert objects resembling prey are also caught and brought out on to land. Woik (1976) also commented on this phenomenon; he found that shrews sometimes carried inedible objects similar to prey from the water to his food rafts, including a lump of peat, sodden flower receptacles, snail shells filled with mud and small twigs. In the wild, then, there may be many wasted dives when such objects are mistaken for live crus- taceans or trichopteran larvae. The energetic cost of foraging underwater may thus be considerable, not only because of heat loss and the physical effort required to sink its buoyant body but also through the necessity to dive repeatedly to catch suitable prey. This would partly explain why wild Water shrews may not take more than about 50°0 of their food from aquatic sources, particularly if, as in Churchfield’s study, prey are small invertebrates. Illing et al. (1981) report that only 5 0 0 of the active period of wild Water shrews is engaged in swimming and diving, the rest is spent in foraging or exploring along the banks beside the water. It is still not known, however, what proportion of dives is successful in locating suitable prey, what the optimum foraging depth is, or whether underwater foraging is more productive than terrestrial foraging; and so research continues.

T o conclude, N. fodiens is unusual amongst mammals because it has the ability to exploit both terrestrial and aquatic environments for food. It also appears to have no special or unusual dietary requirements since it feeds predominantly on common and ubiquitous prey species, Considering its advantages, it remains a mystery why this well-adapted species does not occur moie frequently.

ACKNOWLEDGMENTS I am most grateful to Dr J. Gurnell for his helpful comments during the preparation of this manuscript.

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