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Key words: Copepoda, food, Mesocyclops thermocyclopoides, prey handling time, prey selection, predation, prey
switching
Abstract
In the shallow and eutrophic subtropical aquatic ecosystems, which it generally inhabits, the omnivorous copepod
Mesocyclops thermocyclopoides encounters a wide variety of animal prey types including ciliates, rotifers, and
cladocerans. We studied prey selectivity in laboratory-reared adult females of this species given a choice of (i) prey
types belonging to different taxa (ciliates, rotifers, cladocerans, and cyclopoid nauplii), and (ii) different prey
species within a taxonomic group differing in body size, morphology or behaviour. We also tested the effect of
different proportions of prey species on its selectivity. Prey type proportion had no significant effect on selectivity
of the copepod, nor was there any evidence of switching based on the relative abundance of prey. Among the ciliate
prey species tested, the largest species, Stylonychia mytilus was positively selected regardless of its relative abundance, while the smallest, S. notophora was selected only when its density was higher. Offered a choice of three
species of a brachionid rotifer differing in size, the copepod selected the largest of them, Brachionus calyciflorus,
and avoided the smallest B. angularis. The evasive rotifer Hexarthra mira was also avoided. When prey choice
included three cladoceran species Daphnia similoides, Moina macrocopa and Ceriodaphnia cornuta, the copepod
selected the intermediate-sized M. macrocopa regardless of the abundance of the other two species. Although it
fed on Mesocyclops nauplii when there was no choice, M. thermocyclopoides avoided them when alternative food
was available. In a multispecies prey choice test, the copepod selected predominantly the rotifer B. calyciflorus and
the cladoceran M. macrocopa. We suggest that the prey selectivity patterns shown by M. thermocyclopoides are
adaptive in that they lead to ingestion of the most profitable prey.
Introduction
In many eutrophic water bodies, a wide spectrum of
potential food items including algae, ciliates, rotifers,
cladocerans, and copepod nauplii is available to cyclopoid copepods. Yet, many cyclopoids are known
to feed selectively (Greene, 1983; Williamson, 1986;
Krylov, 1988; Janicki & DeCosta, 1990), exerting a
significant influence on the structure and dynamics of
the plankton community (Karabin, 1978; Kerfoot &
Sih, 1987; Matsumura-Tundisi et al., 1990; Irvine &
Waya, 1993). Prey selectivity in cyclopoids may result
from differential vulnerability of prey species (passive
selection) or from a choice exercised by the predator
of accepting or rejecting a prey item (active selection)
(Stemberger, 1985; Roche, 1990). Since prey vulnerability is a product of preys encounter rates with,
and ease of capture by, the predator (Pastorok, 1981),
certain morphological and behavioural attributes of
different prey species (which influence capturability)
(Li & Li, 1979; Williamson, 1980, 1983a; Stemberger,
1985; DeMott, 1995; Wickham, 1995a,b), and their
relative proportions (which affect encounter rates) in
the medium, may be able to explain observed selectivity patterns in passive prey selection. Active prey
selection has also been demonstrated in some calanoid
and cyclopoid species (Stemberger, 1985; Kerfoot &
Kirk, 1991; Hartmann et al., 1993; DeMott; 1995),
but the mechanisms leading to active selection are not
necessarily the same. In the calanoid Acartia tonsa, for
412
instance, food selectivity is a consequence of two distinctly different feeding mechanisms, ambush feeding
for motile animal prey such as ciliates, and suspension feeding for small immotile food particles such as
diatoms (Kirboe et al., 1996). This suggests that in
omnivorous copepods that regularly include algae in
their diet (Adrian, 1991; Santer, 1993; Santer & Van
den Bosch, 1994; Hopp et al., 1997), their patterns
of animal prey selection might also be related to the
extent of herbivory in them (Adrian & Frost, 1993;
Kumar & Rao, 1999a).
The ability of a predator to switch from one prey
species to another depending on their relative concentrations is an adaptive behaviour that not only allows
the predator to maximize its net energy intake (Landry,
1981) but may also have a stabilizing effect on the prey
population (Oaten & Murdoch, 1975). Prey switching
has been recorded in some calanoid copepods (Landry,
1981; Kirboe et al., 1996) and is implicated in species
that show a Type III functional response (Akre &
Johnson, 1979).
Mesocyclops thermocyclopoides, a common cyclopoid copepod in local ponds and shallow lakes, is
predominantly carnivorous, but with an ability to utilize plant food also (Kumar & Rao, 1999a,b). Our
earlier laboratory studies on food type effects on the
post- embryonic development and reproductive output of this species revealed prey type-related trends
in its survival, longevity and fecundity (Kumar &
Rao, 1998, 1999b). These trends led us to hypothesize
that Mesocyclops thermocyclopoides feeds selectively
based on prey attributes such as body size, shape,
motility, type of movements, and perhaps taste. Further, we asked if selectivity in this cyclopoid is prey
frequency-dependent.
The objective of our present study was to understand the prey selection patterns in the adult female
of M. thermocyclopoides, given a choice of different
prey types including ciliates, rotifers, cladocerans and
copepod nauplii, differing from each other in one or
more of the morphological and behavioural attributes.
Our experiments were also designed to test the effect
of prey proportions in the medium on the selectivity
patterns of the copepod.
413
Table 1. Length, width and dry weight of different prey species used in selection experiments with
M. thermocyclopoides. Values given are Mean SE (n = 20)
Group
Species
Species
abbreviation
Ciliophora
Stylonychia notophora
S. mytilus
Blepharisma musculus
S.n
S.m
B.m
88 10.85
209 20.8
153 28.4
46 7.3
133 15.2
46 15.4
0.008
0.04
0.025
Rotifera
Brachionus angularis
B. rubens
B. calyciflorus
Hexarthra mira
Filinia longiseta
Asplanchna intermedia
B.a
B.r
B.c
H.m
F.l
A.i
88 6.6
149 6.4
197 12.4
160 7.2
98 7.2
745 33.4
77 1.6
135 4.1
155 11.8
51 2.7
0.05
0.16
0.20
0.20
0.20
0.52
Cladocera
Ceriodaphnia cornuta
Moina macrocopa
Daphnia similoides
C.c
M.m
D.s
529 11.0
799 16.4
1446 25.5
363 8.3
456 16.9
804 14.8
3.0
4.60
27.2
Copepoda
Nauplii of
M. thermocyclopoides
98.75 2.5
0.24
Length
(m)
133 4.2
i =
Width
(m)
Dry
weight
(g)
ln(ni0 ri )/ni0
m
ln((nj 0 rj )/nj 0 )
i = 1, 2, 3, . . . , m,
j =1
414
Table 2. Experimental protocols used for tests of prey selection by M. thermocyclopoides (Species abbreviations are
spelled out in Table 1)
Taxonomic group
Test No.
Multi-species choice
13
Prey species
S.n
B.a
B.a
B.a
B.c
C..c
B.m
B.r
F.l
B.c
H.m
M.m
B.c
B.r
S.m
B.c
A.i
Nauplii
Nauplii
Nauplii
Nauplii
Nauplii
Nauplii
S.m
B.m
M.m
M.m
M.m
D.s
M.m
C.c
B.c
B.r
S.n
S.n
B.a
C..c
B.m
B.r
M.m
S.m
B.c
B.c
D.s
S.m
B.c
D.s
Combined prey
density
Volume of
container (ml)
Test
duration
(h)
300
200
200
200
200
30
50
100
100
100
100
100
3
6
6
6
3
12
200
200
100
100
40
40
40
40
120
120
220
100
100
100
100
100
100
100
100
100
100
100
6
6
6
12
12
12
12
12
6
6
3
200
See Table 3.
was offered selected prey species at densities similar to those used in the selectivity tests, and was
continuously observed under a stereomicroscope for
1520 min. The prey handling time (time lapsed between an attack of the prey by the copepod and its
resumption of movement after ingestion) was recorded
to the nearest 0.1 s using a stopwatch. In case of cladoceran prey, the consumption was partial; therefore, the
release of the partially consumed prey by the copepod was taken as the endpoint. For each prey species,
510 individual observations were made to obtain an
average handling time.
Table 3. Prey species and densities used in the multispecies prey selectivity (Test 13)
Species
Stylonychia notophora
S. mytilus
Blepharisma musculus
Brachionus angularis
B. rubens
B. calyciflorus
Ceriodaphnia cornuta
Moina macrocopa
Daphnia similoides
500
250
250
75
50
25
10
6
4
Results
In all the prey choice tests, prey types, but not their
relative proportions, had a significant effect on the
value (two-way ANOVA). However, in many tests
the interaction (prey species proportion) term was
statistically significant, indicating that the effect of relative proportions of the prey on selectivity was prey
type-dependent.
415
Figure 1. Selectivity Index () values for M. thermocyclopoides offered a choice of three prey species belonging to one of the three taxaciliates (a), rotifers (b, c) or cladocerans (d) in different proportions. Values shown are Mean SE (n = 45). The dashed line in each indicates
the value for non-selective feeding. Abbreviated species names are spelled out in Table 1.
416
Prey choice within a taxonomic group
Ciliates (Test 1)
Given a choice amongst S. notophora, B. musculus and
S. mytilus, Mesocyclops showed a strong preference
for the larger ciliate species S. mytilus ( = 0.44
to 0.59, p < 0.01 one way ANOVA), irrespective
of its relative abundance in the medium (Figure 1a).
The smallest species S. notophora was ingested nonselectively except at high relative abundance, when it
was positively selected ( = 0.41, p < 0.05). There
was a significant (p < 0.01) negative selection (avoidance) ( = 0.120.21) for the intermediate-sized
Blepharisma musculus at any proportion.
Cladocerans (Test 6)
A combination of three cladoceran species C. cornuta, M. macrocopa and D. similoidis offered as
food, elicited in Mesocyclops a strong preference for
M. macrocopa ( = 0.6020.718, p < 0.001) regard-
417
Figure 2. Selectivity Index () values for M. thermocyclopoides offered a choice of two rotifer species B. calyciflorus with B. angularis (a)
or with H. mira (b) in different proportions. Values shown are Mean SE (n = 45). The dashed line indicates the value for non-selective
feeding. Abbreviated species names are spelled out in Table 1.
of the prey, the following trends were evident (Figure 5b): (i) the ciliate Blepharisma musculus was
strongly avoided, as could be expected from results of
Tests Ia and IIa; (ii) the cladocerans Ceriodaphnia cornuta and Daphnia similoides were also avoided; and
(iii) the larger rotifer B. calyciflorus and the cladoceran
M. macrocopa were selected positively. The selectivity
values in all three cases were statistically significant
(p < 0.05) against the null hypothesis of random
feeding.
418
Figure 3. Prey selectivity in M. thermocyclopoides offered the choice of a ciliate and a rotifer (a, b), a ciliate and a cladoceran (c), a cladoceran
and a rotifer (d, e) in three different proportions. Values shown are Mean SE (n = 45). The Selectivity Index () value for non-selective
feeding is shown in each case by a dashed line.
419
Figure 4. Selectivity Index () values for M. thermocyclopoides offered Mesocyclops nauplii and an alternative prey type (Abbreviated species
names are spelled out in Table 1). Values shown are Mean SE (n = 45). The dashed line indicates the value for non-selective feeding.
Discussion
Our study demonstrated that Mesocyclops thermocyclopoides is a selective predator. Its selectivity is
probably influenced by important prey attributes such
as size, body shape, taste and behaviour. Although
we did not test it, hunger level of the copepod is
also known to influence prey selectivity (Stemberger,
1985).
The relationship between prey size and prey handling time is helpful in explaining many of the trends
we observed in this study on prey selectivity. For
M. thermocyclopoides prey-handling times increased
exponentially with prey size (Figure 6). Handling
times for ciliates being negligible (<1.3 s), the largest
of them, Stylonychia mytilus was positively selected
regardless of its proportion in the medium, but the
smallest, S. notophora was selected only when its
relative abundance was higher. The higher selectivity of the copepod for S. mytilus was probably due
to its higher encounter frequency and capture probability, which are generally a function of prey size
(Pastorok, 1981; Kerfoot & Sih, 1987). In nature,
size-selective predation by the cyclopoid copepod can
have a marked impact on the ciliate prey community
(Wickham, 1995a,b). The significantly higher mortal-
420
Figure 5. Selectivity Index () values for M. thermocyclopoides offered a combination of different ciliate, rotifer and cladoceran prey species
(a). Manlys Selectivity Index () is also shown separately for the three taxonomic groups (b). Abbreviated species names are spelled out in
Table 1. The dashed line indicates the value for non-selective feeding.
ance of Hexarthra by M. thermocyclopoides suggests that its darting movements offer some protection
against predation, but not those of the other evasive
rotifer Filinia, which was selected for by the copepod
when its proportion was relatively high in the medium.
Contributing to its vulnerability further is the fact that
Filinia, which lacks lorica, requires copepod less handling time (1.83 s) than the loricate B. calyciflorus
(6.43 s). The relatively greater vulnerability of illoricate rotifers to copepod predation has been observed
in many studies (Williamson, 1983b). For Filinia, the
risks of an illoricate body apparently far outweigh any
benefits accruing from its evasive movements, which
may offer some protection only against Asplanchna
(Iyer & Rao, 1996) but not Mesocyclops.
421
Figure 6. Prey handling time and prey profitability (calculated using consumed biomass) in relation to prey body size in M. thermocyclopoides
(all parameters on log-scale). Prey species: 1. Stylonychia mytilus, 2. Filinia longiseta, 3. Brachionus angularis, 4. B. calyciflorus 5. Asplanchna
intermedia, 6. Ceriodaphnia cornuta, 7. Moina macrocopa, 8. Daphnia similoides.
(1983a) observed that prey size per se is not a dependable determinant of copepods preference when
its diet choice includes prey species differing in other
attributes. The main reasons for our caution in interpreting the selectivity index values are: (1) The
selectivity index was calculated using prey numbers,
but when considered in terms of biomass ingested, it
presents an entirely different pattern. (2) M. thermocyclopoides, like other cyclopoids indulges in what is
known as wasteful killing when dealing with largesized cladoceran prey (Monakov & Sorokin, 1959;
Brandl & Fernando, 1975; Krylov, 1988). Daphnia
similoides, by dry weight, is nearly 6 times larger than
Moina. Although M. thermocyclopoides killed more
than 80% of the Daphnia in the container, it utilized
only a few, that too partially. Our gross estimate of the
average percentage of individual biomass left unconsumed was >70% with Daphnia, but less than 40%
with Moina. Thus, for each individual killed, the average dry biomass ingested was 8.2 g for Daphnia,
and 3.2 g for Moina. Further, we get a more realistic
picture of prey profitability if the actual amounts of
the two cladoceran prey ingested were examined in
relation to the respective handling times, another fac-
422
tor influencing prey selectivity (Roche, 1990; Gliwicz
& Umana, 1994). M. thermocyclopoides spent more
than twice the amount of time handling Daphnia than
Moina, making net profitability to the copepod nearly
the same (0.018 and 0.016) for both the prey species
(Figure 6).
When the diet choice included prey types of different taxa, the selectivity patterns in Mesocyclops were
rather different. Given a choice of the ciliate Stylonychia mytilus and the rotifer Brachionus calyciflorus in
different proportions, the cyclopoid selected the more
abundant of the two prey types. This need not necessarily indicate prey switching since, as we argued
in the case of cladoceran prey, biomasses of the two
prey types are not comparable. Indeed, analysis of our
data (using Landrys formula) gives no evidence of
prey switching. However, field studies are necessary to
find out if in local ponds high brachionid rotifer densities tend to relieve Mesocyclops predation pressure on
hypotrich ciliates such as Stylonychia.
Our preceding arguments on Daphnia selectivity
help also to explain the negative selection (avoidance)
that Mesocyclops exhibited for Moina in the Moinaciliate (Figure 3c) and Moina-rotifer (B. calyciflorus)
(Figure 3d) choice tests. Since the weight of one adult
Moina is equal to the combined weight of 115 individuals of S. mytilus, it is evident that the copepod
actually ingested more biomass of the cladoceran than
of the ciliate prey.
The cooccurrence of M. thermocyclopoides with
the predatory rotifer Asplanchna intermedia is not
uncommon in local ponds and small lakes. As both
regularly prey on brachionid rotifers, the observed
efficiency of predation on Asplanchna by M. thermocyclopoides has implications for the population
dynamics of brachionid rotifers in nature. Williamson
& Gilbert (1980) suggested that Mesocylops edax, by
feeding on Asplanchna girodi, could reduce its effect on the rotifer (Keratella cochlearis) prey. We
have no field data to assess the relative importance
of Mesocyclops and Asplanchna predation on Brachionus calyciflorus; however, in a laboratory study
of the dynamics of a two predator (Asplanchna intermmedia and M. thermocyclopoides)-one prey (B. calyciflorus) system, we found that B. calyciflorus persisted
longer in it than in controls with Asplanchna alone
(Kumar & Rao, 2001).
Cannibalism in copepods has been well documented (Landry, 1981; Krylov, 1988; Van den Bosch
& Gabriel, 1991). Although Mesocyclops feeds on
nauplii (of the same species, not necessarily of its own
423
Acknowledgements
We are grateful to William DeMott and two anonymous reviewers for their valuable comments and suggestions on an earlier draft of this paper. We thank
Anupama Kak, J. Vanisree and Anita Nair for technical assistance, and gratefully acknowledge the financial support provided to one of us (R.K.) by the
Council of Scientific and Industrial Research.
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