Freshwater Biology (1995) 34, 21-28

The reaction time of leech and triclad species to

crushed prey and the significance of this for their
coexistence in British lakes
R . M . H . SEABY, A.J. MARTIN A N D J . O . Y O U N G *
Department of Environmental and Evolutionary Biology, University of Liverpool, PO Box 147, Liverpool L69 3BX. U.K.

^Author to whom correspondence should be addressed.

SUMMARY

1. Three species of leeches, Erpobdella octoculata, Glossiphonia complanata and Helobdella

stagnalis, and four species of triclads, Polycelis nigra, P. tenuis, Dugesia polychroa and
Dendrocoelum lacteum, commonly coexist on stony shores in productive British lakes. All
species are food limited and there is much overlap in their diet. For both leech and
triclad communities, coexistence of species is through the occurrence of food refuges.
Leeches are more successful than triclads at capturing live prey, whereas both groups
feed on damaged prey, comprising incapacitated, live or dead animals that are leaking
body fluids. If triclads are better than leeches at exploiting damaged prey, this could be
a mechanism for their coexistence.
2. Laboratory experiments investigated the comparative speeds al which leeches and
triclads responded to crushed prey. Young and adult predators were offered a crushed
specimen of the oligochaete Tubifex tubifex, the snail Lymnaea peregra, the crustacean
Asellus aquaticus or the chironomid Chironomus sp., and their reaction times recorded.
These four prey groups constitute the main diet of the predators in the field. Only D.
polychroa and D. lacteum showed a significantly different reaction time between young
and adults to crushed prey, and the reason for this is unclear. All predators, except H.
stagnalis and D. polychroa, showed a difference in reaction time to the four types of prey,
presumably a consequence of differences in both the 'quality' and 'concentration' of the
different prey fluids, and there were some differences between predators in their speed
of reaction to the same prey type. The following sequence, from fastest to slowest, in
general reaction time to prey was obtained: £. octoculata, D. polychroa, P. tenuis, D.
lacteum, P. nigra, H. stagnalis and G. complanata.
3. The location of the damaged food by the predators can be explained partly in terms
of their foraging behaviour, with E. octoculata, D. polychroa and P. tenuis exhibiting a
more seek-out strategy than other species which have a more sit-and-wait behaviour,
and partly on the leveJ of sophistication of their chemosensory system used to detect
leaked prey fluids. This system is highly developed in triclad species but poorly
developed in leeches.
4. In a second type of experiment in which prey, L. peregra, A. aquaticus or Chironomus
sp., were offered at different time intervals after crushing to H. stagnalis and P. tenuis,
few predators fed on food crushed for 24 h or longer, although a few leeches fed on
Chironomus crushed for up to 72 h.
5. It is concluded that coexistence of leech and triclad species on stony shores in lakes is
assisted by partitioning of food on a damaged or live basis.
© 1995 Blackwell Science Ltd 21
22 R.M.H. Seaby, A.J. Martin and J.O. Young
Introduction
The most numerous invertebrate predators inhabiting
the stony littoral zone of British productive lakes
comprise a guild of leech and triclad species (Reynold-
son, 1966; Young & Ironmonger, 1981). The common
species include the leeches Erpobdella octoculata (L.), 10 mg) and the triclads P. nigra (7-8 mm body length
Glossiphonia complanata (L.) and Helobdella stagnalis (L.), in gliding movement; 6-7 mg wet weight), P. tenuis
and the triclads Polycelis nigra (Mull), Polycelis tenuis (7-8 mm; 6-7 mg), D. polychroa (9-10 mm; 8-9 mg) and
Ijima, Dugesia polychroa (O. Schmidt) and Dendrocoelum D. lacteum (14-16 mm; 23-26 mg) were collected from
lacteum (Mull.). Populations of all these species are
food limited (Reynoldson, 1983; Martin, Seaby &
Young, 1994a), and field studies have demonstrated
much overlap in their diets, which include oligo-
chaetes, molluscs, crustaceans and insects (Reynoldson
& Davies, 1970; Reynoldson, 1975; Young, 1981; Young
& Spelling, 1989). However, within each of the triclad
and leech communities, each genus has a food refuge,
that is, a prey taxon on which it feeds to a greater
extent than do the other genera (Reynoldson & Davies,
1970), and this allows their coexistence (Reynoldson,
1966, 1983; Young & Spelling, 1989). The question
arises as to how leech and triclad species can coexist,
given the considerable overlap in their diets; for
example, both D. polychroa and G. complanata feed
extensively on molluscs.
Laboratory studies have shown that leeches are far
more successful than triclads at feeding on intact live
prey organisms, but that both feed on damaged prey
comprising incapacitated live or dead animals that
are leaking body fluids (Reynoldson & Young, 1963;
Martin, Seaby & Young, 1994b). If triclads are more
successful in locating and exploiting damaged prey
than leeches, then coexistence might be permitted
through the division of the food niche in terms of
damaged or live prey. Unfortunately, field studies on
diet only identify the type of prey eaten and not its
condition.
Little is known about the comparative ability of
leeches and triclads to detect and react to damaged
prey, and the present work was designed to answer
the following questions. Does the type of prey and
age of the predator (leech or triclad species) affect the
predator's reaction time to crushed food? Is there a
difference in reaction time to a particular food between
different predator species? Does the length of time a
prey organism has been dead have an effect on the
feeding behaviour of the predator?
Material and methods
Experimental procedure
Adults of the leeches E. octoculata (17-18 mm body
length at rest; 30-32 mg wet weight), G. complanata
(12-13 mm; 20-22 mg) and H. stagnalis (8-9 mm; 9-
Crose Mere, an ion-rich, productive lake in Shropshire
(Nat. Grid Ref. SJ 430 305). Some specimens of each
species were starved for 10 days prior to their use in
experiments. Others were cultured in the laboratory,
at 14 °C using a natural photoperiod, to produce
young which were used in experiments soon after
hatching from cocoons (E. octoculata and triclad
species) or release from parents (glossiphoniid
leeches).
Oligochaetes, molluscs, crustaceans and chironom-
ids constitute the major components in the diet of the
predators in the field (Reynoldson & Davies, 1970;
Young, 1981; Young & Spelling, 1989). Accordingly,
the four prey species used in experiments were the
oligochaete, Tubifex tubifex (Mull.) (20-22 mm body
length), the gastropod mollusc Lymnaea peregra (Mull.)
(10-12 mm), the isopod crustacean Asellus aquaticus
(Linn.) (10-12 mm) and the chironomid Chironomus
sp. (10-12 mm). The first and last species were obtained
from an aquarium shop in Liverpool, and the others
from ponds on Merseyside. All experiments were
conducted at 14 °C, an optimum temperature for all
the predator species (Reynoldson, Young & Taylor,
1965; Young & Ironmonger, 1982), under natural light
conditions.
Crystallizing dishes of 7 cm diameter and 200 ml
capacity were three-quarters filled with lake water
from Crose Mere. A single predator was placed in
each dish and allowed to acclimatize for 30 min.
Almost always, the predator came to rest at the edge
of the dish in the angle of the wall and the floor. If it
did not, the dish was discarded. An immobilized prey
individual, crushed by a single uniform squeeze using
a forceps, was introduced gently to the centre of the
floor of the dish, avoiding physical disturbcince of the
water. The time taken for the predator to find and
start feeding on the prey was recorded in seconds.
Observations were continued for up to 1 h. For each
predator and prey combination, thirty replicates were
© 1995 Blackwell Science Ltd, Freshwater Biology, 34, 21-28
 Leeches and triclads 23
Table 1 The mean reaction times (s), with standard deviations in parentheses, of adult and young leeches and triclads to various
crushed prey species, n = 30, except for Dendrocoelum lacleum for which n = 20. Because only two adull and two young D. lacteum
fed on Lymnaea peregra, mean times are not shown. Young Polycelis nigra were not used.
Eo = Erpobdella octoculata; Gc = Glossiphonia complanata; Hs = Helobdella stagnalis; Pn = Polycetis nigra; Pt = Polycelis tenuis; Dp =
Dugesia polychroa; Dl = Dendrocoelum lacteum; Tt = Tubifex tubifex; Lp = Lymnaea peregra; Aa = Asellus aquaticus; Ch = Chironomus
species

Predator species

Prey
species Eo Gc Hs Pn Pt Dp Dl

Adults
Tt 156.67 404.53 ,195.00 191.13 177,57 163.47 185.10
(65.16) (274.99) (275.90) (104,23) (103,39) (115-10) (111.27)
Lp 315.07 331.73 379,33 612,63 741.13 158.83 -
(143.74) (195.13) (226-20) (899.67) (1056.52) (98.78) -
Aa 175.77 499.43 443.70 183.07 164.27 169,23 166.80
(72.64) (336-90) (384.93) (106.90) (102.22) (122.75) (104.83)
Ch 141.73 460.53 431.73 186.73 167.10 187.10 228.80
(68.66) (297-02) (269.19) (162.60) (94.92) (123.96) (85.79)

Young
Tt 161.77 435.10 435.57 - 194,97 212.13 223.30
(69.18) (319.05) (349.51) - (100.78) (135.35) (109.54)
Lp 359.63 399.77 438.60 - 883.30 182.40 -
(147.29) (260.86) (285.86) (1198.95) (102.13) -
M 193.17 552.67 507.10 - 196.47 203.37 218.15
(67-88) (374.69) (407.47) - (110.10) (120.09) (117.54)
150,40 510.10 505.38 - 221.40 211.40 292.85
(59,60) (346.13) (335,18) - (128.68) (138.69) (79.27)

used with the exception of D. lacteum where there
were only twenty. Young P. nigra could not be tested
as insufficient numbers were obtained.
In experiments which investigated the attraction of
decaying crushed food, a single crushed prey was
introduced to the centre of the floor of each of 105
dishes of 7 cm diameter and 200 ml capacity and three-
quarters filled with lake water. The body fluids of the
crushed prey had diffused throughout the experi-
mental arenas in less than 30 min, as witnessed by the
leaking of red haemoglobin from Chironomus. The
dishes were divided into seven groups of fifteen. Each
group was left for either 30 min or 3, 5, 16, 24, 48 or
72 h before a single predator was introduced, using a
spatula, into each dish at its edge in the angle of the
wall and the floor. The predator was then observed
for 30 min to see if it fed. The experiment was repeated
for each of the prey types L. peregra, A. aquaticus and
Chironomus sp., and each of the predators H. stagnalis
and P. tenuis. Only adult predators were used.
Analysis of data
A two-way ANOVA was used to test for differences
in reaction time within a predator species with regard
© 1995 Blackweil Science Ltd, Freshwater Biology, 34, 21-28
to age of predator and prey type. When a significant
difference was obtained a Tukey least significant differ-
ence test was performed (Zar, 1984). To test for differ-
ences between predator species in reaction times to
each of the four prey types, a one-way ANOVA was
carried out for each food type followed by a Tukey
test where results were significantly different. Data for
young and adult predators were analysed separately.
Results from the experiment investigating the effect
of decaying food on predator response were analysed
using the chi-squared test. For each food type, compar-
ison between the two predatory species was made at
each time interval.
Results
V^itJtin-species reaction times
Erpobdella octoculata reacted significantly more slowly
to L. peregra than to the other prey types which did
not differ from each other {Tables 1 and 2). There was
no difference between ages. For G. comptanata, there
was no significant difference between ages. Its
response times to L. peregra (fast) and A. aquaticus
(slow) were significantly different, with intermediate
24 R.M.H. Seaby, A.]. Martin and J.O. Young
Table 2 Results of two-way ANOVAs
Predator Age of predator Prey type to test for differences in reaction times
Significance level Significance level Tukey test prey groupings within a predator species to four
different prey types, with regard to age
Eo NS < 0.001 Tt Aa Ch of predator and prey type. Tukey test
Ge results also show significantly different
m <0.05
NS
Tl Iv Ch TtAaCh
groupings of prey types. Young
m
p»
m < 0.001 Tt Aa Ch Polycelis nigra were not used and so
Pt
-NS < 0.001 Tt Aa Ch few Lymnaea peregra were eaten by
<0.05 NS Dendrocoelum lacteum that data are not
Dl <0.01 <0.01 TtAa Ch included in calculations. Predator and
prey abbreviations as in Table 1

Table 3 Tukey test results showing significantly different of the four prey types, T. tuhifex, A. aquaticus and
groupings of predators for each of four prey types. A, adult
predators; Y, young predators. Predator and prey Chironomus sp. (Tables 1 and 3). Glossiphonia complanata
abbreviations as for Table 1 and H. stagnalis were significantly slower to find these
food types than were the other predators between
Prey
Species Predator species which there were no significant differences. Dugesia
polychroa reacted faster to L. peregra and was signific-
Tt A Eo Pn Pt DpDl GcHs antly different to both P. nigra and P. tenuis, which
Y Eo Pt Dv Dl GcHs
Aa A Eo Pn Pt DvDl Gc Hs were the slowest, and to an intermediate group com-
Y Eo Pt Dp Dl GcHs prising the three leech species. Dendrocoelum lacteum,
Ch A Eo Pn Pt DpDl GcHs which fed sparingly on L peregra, was not included
Y Eo Pt Dv Dl GcHs
Lp A in the analysis.
Eo Gc Hs PnPt
Y Eo Gc Hs Pt Bearing in mind that young P. nigra were not used
in experiments, the results for the young predators
were similar to those for the adults. No young D. lac-
reaction times to Chironomus and T. tubifex, which teum fed on L. peregra in the experiments.
were inseparable from either L. peregra or A. aquaticus. When the predators were ranked in order of reaction
HeJobdella stagnalis showed no significant differences
time to each prey type and then these ranks summed
between reaction times for age or food type. The
for each predator species, the following sequence of
response time of P. nigra to L peregra was significantly
predators, in terms of increasing reaction time, for
slower than to other prey types between which there
both adults and young, was obtained: £. octoculata, D.
was no difference. For P. tenuis there was no significant
polychroa, P. tenuis, D. lacteum, P. nigra, H. stagnalis and
difference with respect to age. Reaction time to L
G. complanata (Table 4).
peregra was significantly slower than to the other food
types which showed similar reaction times. Dugesia
polychroa showeci no difference in reaction time to any
Response to decaying food
prey type but young were sigruficantiy slower than
adults to feed. Young D. lacteum reacted significantly In experiments investigating predator response to
slower than adults to prey. For both age-groups, decaying crushed prey, the number of predators, for
response times to Chironomus were slower than to T. both H. stagnalis and P. tenuis, which fed within a 30-
tubifex and A. aquaticus. So few L. peregra were attacked min period on A. aquaticus that had been crushed and
that they were not included in the analysis. had decayed for various time intervals, remained fairly
similar up to 16 h after crushing (Fig, 1). At 24 h,
numbers declined dramatically, with none feeding at
Between-species reaction times
48 h. At none of the time intervals was there a signific-
For both young and adults, significantly different ant difference between the numbers of H. stagnalis
reaction times between predator species to each of the and P. tenuis feeding. When exposed to L peregra, the
four prey types were obtained, and so, in the interest numbers of leeches and triclads which had fed
of space, orJy Tukey test results are shown in Table 3. declined gradually with only a single P. tenuis feeding
Adult reaction times were very similar for three out on L peregra which had been crushed 48 h earlier.
© 1995 Blackweil Science Ltd, Freshwater Biology, 34, 21-28
 Leeches and triclads 25
Table 4 The ranks of the leech and triclad reaction times (cf.
15
Table 1) and the sums of the ranks for all prey types, for adult
and young predators. Young Polycelis nigra were not tested. (a)
Predator and prey abbreviations as for Table 1
10
Predator species

Prey species Eo Dp Pt Dl Pn Hs Gc

Adults
Tt 1 2 3 4 5 6 7
Lp 2 1 6 7 5 4 3
Aa 4 3 1 2 5 6 7 15
Ch 1 4 2 5 3 6 7
Sum 8 10 12 18 18 22 24 (b)

Young
Tt 1 3 2 4 - 6 5
Lp 2 1 5 6 - 4 3
Aa 1 3 2 4 - 5 6
Ch 1 2 3 4 - 5 6
Sum 5 9 12 18 - 20 20

Again, there were no significant differences between 15

the number of H. stagnalis and P. tenuis feeding at any (C)
of the time intervals.
When exposed to Chironomus, H. stagnalis fed on 10

food which had been left for a longer period of time

after crushing than did P. tenuis which ceased feeding
on prey after it had been crushed longer than 24 h.
One leech fed when exposed to a chironomid which
had been crushed for 72 h. At 24 h, and subsequent
time intervals, significantly more H. stagnalis fed than
did P. tenuis.
Discussion
In the present experiments, for both young and adult
animals, £. octoculata and all the triclad species reacted
relatively more quickly to the presence of crushed
food than did the two glossiphoniid leeches. The
location of food by the predators will depend on
their foraging strategy and their ability to detect
the presence of prey. Schoener (1971) suggested two
extreme types of foraging behaviour, namely, 'sit-
and-wait' and 'search-out'. In common with other
erpobdellid leeches, £. octoculata is an active, although
clumsy, hunter, and the only predator tested in the
current experiments which is capable of swimming
(Greene, 1974; Davies et al, 1982; Anholt & Davies,
1986; Yoimg & Spelling, 1989), whereas the glossi-
phoniid leeches, G. compJanata more so than H. stag-
nalis, have a relatively more sit-and-wait strategy
(Wrona & Calow, 1988; Young & Spelling, 1989; Young,
© 1995 Blackweil Science Ltd, Freshwater Biotogy, 34, 21-28
72
Fig. 1 The number of predators, adult Polycelis tenuis {Pt) or
Helobdella stagnalis (Hs), which had fed within a 30-min period
on crushed prey, Asellus aquaticus (a), Lymnaea peregra (b) or
Chironomus sp. (c), which had been dead for various lengths of
time. « = 15 for each predator-prey combination.
Martin & Seaby, 1993). Of the flatworm species, P.
tenuis and D. polychroa have been shown to be more
active predators than D. lacteum and P. nigra (Reynold-
son & Young, 1963; Bellamy & Reynoldson, 1974;
Calow & Wooilhead, 1977; Calow, 1980; Calow & Riley,
1980; Reynoldson, Gilliam & Jaques, 1981; Herrmann,
1984). Thus, differences in feeding strategy may con-
tribute in part to an explanation of the present findings.
The ability to detect the presence of prey will depend
on the level of sophistication of the predator's sensory
system. Distance of predator from food source, an
important component of detection, was standardized
in the present experiments. However, when actively
searching for food E. octoculata can greatly extend its
resting body length, and its large size, relative to the
other predators, may have resulted in artificially fast
26 R.M.H. Seaby, A.j. Martin and j.O. Young
reaction times being obtained for this leech, as it
would, by chance alone, be more likely to make contact
with a food item in the small experimental arenas
used. Certainly, this should be borne in mind in the
interpretation of the results.
Triclad species are well endowed with chemorecep-
tors by means of which food emitting body fluids
are readily detected (Hyman, 1951). These, although
scattered over the entire body, are particularly concen-
trated in the anterior auricular grooves. The presence
of intact live prey is detected either by direct contact
with chemoreceptors or by the disturbances created
in the water by the prey. Ciliary tactile receptors
are distributed over the entire body with particular
concentrations on the body margins and auricles. In
contrast to triclads, chemosensory cues play a much
lesser role in prey detection by leeches, with chemosen-
sory ability mainly restricted to situations when the
animal is in physical contact with its prey (Davies
et al, 1982; Sawyer, 1986). Erpobdelk montezuma Davies,
Singhal & Davies, a predaceous leech that undergoes
a twilight migration into the surface waters of
Montezuma Well, Arizona, uses mechanoreception to
forage on pelagic amphipods (Blinn, Wagner & Grin,
1986; Blinn, Pinney & Wagner, 1988). However, most
erpobdellid leeches appear to encounter prey by
chance but once contact has been made tactile and/
or chemoreceptors are important in the selection and
handling of the prey (Greene, 1974; Davies etal, 1982;
Blinn & Davies, 1989). Thus, differences in the sensory
systems used to detect prey between leeches and
triclads would also contribute to an explanation of the
present experimental findings. Because the offered
food comprised recently crushed prey which leaked
fluids, the triclads would be at an advantage, locating
prey in advance of leeches. However, as stated above,
the fast response time of the erpobdellid was most
likely due to a combination of its active hunting
strategy and large size relative to the size of the
experimental containers used.
For each predator species, reaction times of young
and adult animals were similar, with the exceptions
of D. polychroa and D, lacteum for which young were
sigruficantiy slower. The reason for this is unclear, but
the presence of fewer sensory cells in and/or the
reduced locomotory ability of the smaller animals may
be implicated.
For each predator, with the exception of H. stagnalis
and D. polychroa, there were differences in the speed
of reaction to different prey Also, there were some
differences between predators in their speed of reac-
tion to the same prey type, which is of greater relevance
to the question of coexistence. The speed of arousal
to prey by triclads, and discrimination between prey
by both leeches and triclads would be governed by
both the 'quality' and 'concentration' of the prey
fluids. Both of these attributes are difficult to measure,
and this was not attempted in the present study.
Lymnaea peregra was least 'attractive' to the predators,
with the exception of G. complanata, H. stagnalis and
D. polychroa. Interestingly, these predators, particulariy
G. complanata and D. polychroa, have a large component
of snails in their diet in the field (Reynoldson &
Davies, 1970; Young, 1981; Young & Proctor, 1986;
Young & Spelling, 1989). Because the snails were
crushed in the present experiments, the presence of
a shell and htehavioural defences such as shaking
(Townsend & McCarthy, 1980; Bronmark & Malmquist,
1986; Brown & Strouse, 1988) could not have been
involved in deterring attacks by the other predators.
However, it is possible that mucous production,
evident during the crushing process, may have been
implicated. The present findings are in broad agree-
ment with those of Bellamy & Reynoldson (1974)
who observed the response of triclads to prey juices
dropped into experimental arenas; the fluid of the
snail Potamopyrgus jenkinsi (Smith) was least attractive
to the triclads.
The concentration of leaked fluids from a crushed
prey organism will diminish with time and the stimu-
lus for predation using chemosensory cues will be
reduced. Also, the process of tissue decay will com-
mence on death and the palatability of the food may
change. Certainly, in the present experiments, the
number of leeches and triclads feeding on crushed
prey declined with time, with few feeding on prey
which had been killed for 24 h or longer. Exceptionally,
H- stagnalis fed on chironomids which had been
crushed for up to 72 h, and reasons for this can only
be speculative.
It is concluded that differences in ability to capture
live prey, foraging strategies, and in the detecfion of
damaged prey will contribute to the coexistence of
lake-dwelling leeches and triclads. Leeches are more
efficient than triclads at catching live prey due to the
possession of suckers and in the case of £. octoculata
to its macrophagous feeding habit (Reynoldson &
Young, 1963; Martin, Seaby & Young, 1994b). Triclads
© 1995 Blackwell Science Ltd, Freshwater Biology, 34, 21-28

lack suckers and find live prey, with the excepfion of
less vigorous, soft-bodied prey such as oligochaetes,
difficult to catch. Exceptionally, D. lacteum with its
anterior 'pseudosucker' and through the production
of mucous traps is able to capture live prey such as
Asellus (Reynoldson & Young, 1963; de Silva, 1976).
The glossiphoniid leeches, parficularly G. complanata,
and 0. lacteum exhibit a more sit-and-wait feeding
strategy than E. octoculata and the other triclad species,
capturing active prey which arrive in their vicinity
and presumably reducing the energy costs of active
foraging.
Triclads can exploit damaged prey, including incapa-
citated, live or recently dead animals that are leaking
body fluids, better than leeches. The fast reaction times
of triclads to damaged prey can be explained in terms
of a highly developed chemosensory system and their
active foraging strategy, parficularly with regard to
the dugesiid and planariid species. Leeches have a
poorly developed chemosensory system and this,
together with the more sit-and-wait feeding strategy
of the glossiphoniids, results in a lesser ability to
utilize damaged prey. The fast reacfion time of £.
octoculata in the present experiments was due to its
acfive, although random, foraging strategy.
Acknowledgments
Thanks are expressed to the Natural Environment
Research Council for financing this work, to Professor
T. B. Reynoldson and an anonymous referee for helpful
comments on the text, and to the owners of Crose
Mere and English Nature, Shrewsbury for permission
to sample leeches and triclads.
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