Download complementary feeding niches sustained by size

COMPLEMENTARY
FEEDING
BY SIZE-SELECTIVE
NICHES SUSTAINED
PREDATION1
Stanley I. Dodson
Department
of Zoology,
University
of Washington,
Seattle
98105
ABSTRACI’
A study of the planktonic
communities of 24 similar ponds in the mountains of Colorado
supports the hypothesis that one predator population
can sustain another as a result of sizeselective predation on the prey of both predators.
A highly selective predator excludes its
preferred
(large)
food items and thus favors the presence of suboptimal
(smaller-sized)
prey populations
which are the preferred
food of the second, dependent, predator.
The
suboptimal prey species are found only with size-selective predators, and it is probable that
these are the only suitable prey species for the dependent predator.
This interaction
can
occur in simple communities but also appears to be common in more diverse, complex communities. To support the discussion of this interaction,
the electivity
coefficients
and predation pressures of three freshwater planktivores
were estimated.
INTRODUCKCON
Major characteristics of a community are
the number, identity, and density of the
various species; these are affected through
the interaction of predation, competition,
and chance processes against the background of the physical environment.
Predation acts through
its intensity
and
selectivity.
HrbiEek (1962) reviewed evidencc of the effect of fish predation on
zooplankton species composition and presented observations supporting the effect.
Brooks and Dodson (1965) showed a relationship between the size-selective predation pattern and the specific zooplanktonic
composition in aquatic communities, and
Brooks (1968) measured experimentally the
relative size-selective feeding pattern of
the fish Alma pseudohmangus. This predator-prey relationship based on predation
patterns can be extended to include interactions between predator species; Paine
( 1966) showed that the removal of a “keystone” predator species from a marine intertidal community resulted in a reduction of
the number of herbivore and carnivore
species in the community.
I hypothesize
that size-selective predation affects the diversity of predator as well as prey species
in freshwater planktonic communities. This
effect can be demonstrated in very simple
communities consisting of four or fewer
major animal species on the herbivore and
primary carnivore trophic levels. It has
been observed in planktonic co8mmunities
of a series of small ponds at high altitudes
in the mountains of western Colorado, in
which some combination of the three most
common herbivores and the three common
predators makes up the simple zooplanktonic community of each pond.
Fieldwork
was done from the Rocky
Mountain Biological Laboratory ( Gunnison
Co.), Colorado. An important study area
containing several ponds was the laboratory’s newly acquired Mexican Cut (the
Nature Conservancy’s “Galena Mountain
Project”) biological preserve.
MATEXIALS
AND
METHODS
More than 50 small ponds in the mountains around the Gunnison River Basin and
l This research, was supported by National Scion Grand Mesa, Colorado, were sampled
ence Foundation
Undergraduate
Research Program
from 1965 to 1969. Of these, 24 were quangrants from Yale University
during the summers of
1965 and 1966, and by a N.D.E.A.
Title IV Feltitatively sampled several times during one
lowship
and an N.S.F. Ecology
Training
Grant
to three summers. The ponds are all seep(both from the University
of Washington)
from
age
ponds above 2,700-m elevation, have
1966 to 1969. This paper is condensed from a
large areas of open water (relative to
Ph.D. thesis to be submitted to the Department
of Zoology of the University
of Washington.
emergent vegetation), and lack fish.
131
132
STANLEY
Qualitative
samples were taken by repeatedly towing a No. 20 plankton net
through all depths of these generally shallow ponds. Series of quantitative samples
were collected by pumping 8 or 12 liters
of middepth water through a No. 20 plankton net at evenly spaced intervals along the
ponds longest axis. The major zooplankters
were identified, and size ranges were measured to the nearest 0.033 mm with an eyepiece micrometer in a binocular dissecting
microscope. The population size distributions for the Daphnia species were estimated by measuring the total length (to
the nearest 0.033 mm) of about 200 haphazardly selected individuals from each set
of samples.
Bailey’s triple catch method
(Bailey
1952) for small samples was used to estimate the size of larval salamander (Ambystoma tigrinum)
populations.
Clipped
toes marked the larvae for recapture. Three
ponds containing salamander populations
were carefully surveyed and their volumes
estimated. Thus, the salamander predation
pressure could be calculated on a per liter
bmasis.
Estimates of the larval salamander predation pattern were made from the analysis
of stomach contents. On each sampling
date, three or more larvae were killed, their
stomachs opened, and the species therein
identified and counted. Any Daphnk-z present were also measured. Field observations
and feeding experiments show that the
salamander larvae feed only during the day
and mostly during the morning hours.
They were therefore collected in the early
afternoon when their stomachs still contained the entire day’s meal, permitting a
direct estimate of feeding rate.
Feeding experiments provided estimates
of the predation pattern of two species of
the larval midge Chaoborus. These experiments were done at the University
of
Washington, where the Colorado Chaolborz~s is not available. However, there is no
reason to suspect that these laboratory observations depart qualitatively
from the
Colorado midge’s natural predation pattern.
A single well-fed fourth instar larva of
I.
DODSON
Chaoborus nyblaei or C. fluvicans was
placed in a glass vessel with a culture of
reproducing Daphnia pulex. After 24 l-n- at
2OC, and 12 hr of light, the animals were
killed and measured. The Daphnia which
had been eaten by the Chuoborus were reduced to balls of chitin, so the original total
length of these animals was estimated by
measuring the length of the postabdominal claw. (There was a linear correlation
between the claw length and total length
with a correlation coefficient greater than
0.95.) The experiments were done first in
vessels of 30 ml, then 200 ml, with average
Daphniu densities of 57 to I70 per liter.
The statistic used to measure the predators’ selectivity is described but not recommended by Ivlev ( 1901). It is calculated
by dividing the available and eaten size
distributions into corresponding size classes,
which in this case correspond to daphnid
instars. For the ith size class, the percentage of individuals
taken by the predator
(r$) is divided by the percentage of all
individuals
(~4) available to the predator:
E = ri/pu. E is equal to unity if the predator is acting nonselectively by taking food
in the same proportion as it is available.
Values of 0 to +l indicate avoidance ( taking food in lesser proportion than available ) , and values of +1 to + a indicate
preference (taking food in greater propor
tion than available).
Preference is synonymous with the “positive selectivity”
or
“electivity”
of Ivlev ( 1961) and “predator
interest” of Brooks ( lQ68), avoidance with
lack of selectivity or electivity and lack of
predator interest. Ivlev prefers a different
coefficient, E’, calculated as E’ = (rt - pi)/
( r4 + pi), because it is finitely bounded and
evenly distributed about zero. Zero indicates nonselective feeding; values from -1
to 0 indicate avoidance, and values from
0 to +I indicate preference. For general
use, E is more versatile than E’. Ratios of
the E coefficients for different predators
( with the same available prey) are equivalent to ratios of the relative selectivity of
the predators, although the E’ coefficients
are not related in any simple way. Also,
for purposes of graphic representation of
,
SIZE-SELEC’ITVE
TABLE 1.
Dominant zooplanktonic species in 24
Colorado ponds
Size range (mm)
Species
1911; larvae
(snout-vent)
Chaoborus americanus
(Johannsen, 1903);
instars III & IV
i
larval
6-11
(total
length)
Diaptomus shoshone S. A.
Forbes,
0.2-3.0
1893
Herbivores
Branchinecta coloradensis
0.2-12
Packard, 1874
Daphnia pulex
Leydig,
Emend.
1860”
Richard, 1896
Daphnia rosea Saw, 1862”
Emend, Richard, 1896
0.7-3.0
0.4-1.5
Diaptomus coloradensis
Marsh,
0.1-1.2
1911
* As Brooks (1957)
also found, many Daphnin pogulations in western North America closely resemble D. pulex
Leydig, but are yet distinctly different.
Some populations
in my study ponds resembled D. minnehaha Herrick 1884,
a species not accepted by Brooks ( 1957), who considered
it a form of D. pulex Leydig.
I also found undescribed
populations with morphological
variations from the typical
D. rosen Sars. However, since the variations are very small,
all daphnid populations
in this study are referred to as
either D. pulex or D. rosea.
E coefficients, log E has the range of avoidance equal to that of preference ( as does
E’). Therefore, I have chosen to use the
E coefficient.
An electivity function is a
set of coefficients for the size classes of a
population size distribution.
RESULTS
The major species and their size ranges
are listed in Table 1. These species are
found in two general community types,
represented as A and B, depending on the
presence or absence of actively feeding
salamander larvae (Table 2).
The major differences between the two,
communities are that the herbivorous species of A are smaller than those of B and
that A .contains two predators, while B
contains one. Rotifers, (represented by 5
major ubiquitous species in the 24 ponds)
were about 10 times as dense in the type
A ponds as in type B ponds. Populations
of Sida crystallina (0. F. Muller, 1875),
The two zooplanktonic communities
found in 24 Colorado ponds
No. onds containing
alB these species
Species
Chaoborus americanus
Ambystoma tigrinum
Daphnia rosea
Diaptomus coloradensis
Daphnia pulex
Diaptomus shoshone
Branchinecta coloradensis
A
6-75
only
2,
TABLE
Community
Predators
Ambystoma tigrinum Gary,
133
PREDATION
B
r
I
l2
1
3
ubiquitous
8
I
’
1
Ceriodaphnia, Holopedium, and other small
cladoceran species are occasionally common in type A communities, but never in
type B communities.
Of the 15 type A communities, 13 are
preceded by type B communities when
there are no active salamander larvae in
the pond. Depending on their life cycle in
each pond, salamander larvae are usually
absent or at low densities between the time
of the spring thaw and the early summer
months. In all 13 ponds, the type A community replaces type B during the first
few weeks of larval salamander development (beginning in early summer). During
the period of increasing salamander predation, type B species form resting eggs at the
same time that resting eggs of the type A
( crustacean) species are hatching.
Chaoborus larvae are present all year, but
recruitment occurs only when type A species are present. Table 3 shows the relative
frequency of the large D. pulex (D. mlinnehctb-like
form) in Leechmere ( Gunnison Co., Colorado)
and in the larval
salamanders’ diet during the time of transition from the type B to type A community,
In the 9 ponds which do not contain larval salamanders, type B communities persist
TABLE
3. The relative frequency of Daphnia
pulex as per cent of the total Daphnia,
Leechmere, 1968
Date
9 Jul”
19 Jul
29 Jul
8 Aug
* The salamander
In plankton
(%I
In salamander
diet (%)
38
35
38
11
11
0.5
eggs hatched
19
5
on about this date.
134
STANLEY
TABLE
The feeding rate of salamanders in
4.
Leechmere, 1968
Old generation
---
25
9
19
29
13
28
12
I*
Jun
Jul
Jul
Jul
Aug
Aug
Sep
4
4
4
3
1
11-k
4
65
45
102
10
IrI*
-.
1,275
1,250
1,217
1,209
1,179
0
0
5
~-
3
2
3
11t
The feeding rate of two species of
Species
111s
50 est. 11,420
75 est. 10,290
110
9,370
101
7,910
34
6,445
5,388
34
all summer. Only one species (Diaptomus
coloradensis) occurs in both communities,
and except during a short transition period,
only one or the other of these two sets of
spccics will be present.
Stomach analyses showed plankton to be
the major food of salamanders only during
the first few weeks of development. After
this, plankton makes up less than lo;/, of
the diet; the larger part is composed of
insect larvae and amphipods. Chaobor~
larvae and pupae are a significant component of the diet, and most midge mor-
I*
C. flavicans
C. f lavicans
C. nybluei
* I:
t II:
j: III:
0 IV:
oborus.
per day
III*
w-
170
2.4
44
3:9
_~ 11-t
30
200
200
7
13
z7”
Number of trials.
Size of the experimental
vessel in milliliters.
Effective daphnid concentration
(per liter).
Number of Daphnia pulex eaten per day per ChaNote that an average of 3.2 Daphnia were eaten
by C. flnvicnns.
tality is due to salamander predation.
Copepods are seldom eaten.
Although larval salamander feeding rates
and elcctivity
coefficients were gathered
over four summers from 3 ponds, only a
representative set from the 1968 Leechmere
samples is given (Tables 4 and 5). The
electivity coefficients in Table 5 are for
the average salamander stomach content on
each date. In this pond, the salamander
larvae develop from egg to adult in 1 yr,
with the transformation
occurring in the
end of July or early August.
The fourth and probably the third larval
instars of Chaoborus spp. feed exclusively
on zooplankton (Berg 1937). ChaoboYmCs
americanus feeds about equally on the
larger developmental stages of D. colora-
Representative electivity coefficients of salamander larvae from Leechmere, 1968
__~
p_p_p.-.--L.
Date
Avg snout-vent
salamander
length (cm)
9 Jul
6.8
19 Jul
6.
Chaoborus
New generation
1*
* I: Number of salamander larvae examined.
t II: Average number of Daphnin eaten per salamander
per day.
4: III:
Estimated number of salamanders in the pond.
Censuses were taken on two dates in 1967 and on 8 July
and 30 August in 1968. The other values are interpolated.
TABLE 5.
TABLE
-
_Date
I. DODSON
7.0
Electivity coefficient, above the weighted
mean of the prey size class (mm)
0.09
0.18
0.57
0.70
0.50
0.94
1.32
1.14
5.85
1.51
10.4
1.88
31.0
2.14
0.00
0.00
0.57
0.67
0.42
0.80
0.96
1.04
3.18
1.27
3.86
1.51
13.3
1.81
29 Jul
7.3
0.06
0.50
0.15
0.67
0.25
0.80
1.64
1.01
2.23
1.24
2.05
1.37
2.07
1.61
29 Jul
1.9
0.07
0.50
0.28
0.67
0.71
0.80
1.97
1.01
2.49
1.24
2.33
1.37
1.87
1.61
13 Aug
3.2
0.03
0.50
0.14
0.64
0.78
0.77
2.03
0.97
5.61
1.27
2.90
1.51
0.93
1.71
28 Aug
3.9
0.00
0.54
0.23
0.64
0.34
0.77
0.85
1.01
1.72
1.21
3.26
1.44
3.27
1.44
12 Sep
4.6
0.00
0.50
0.00
0.64
0.50
0.84
1.49
0.97
_----_-.-
3.03
1.17
2.23
1.44
--
SIZE-SEL~ECTIVE
TABLE 7.
Electivity
135
PREDATION
coefficients of the fourth instars of two species of Chaoborus
Electivity coefficient, above the weighted
mean of the prey size class (mm)
Species
Avg total length
(mm)
C. f lavicans
12.0
1.74
0.67
0.98
0.84
2.81
1.04
1.26
1.31
0.18
1.61
0.00
1.98
0.00
2.24
C. nyblaei
14.5
0.88
0.67
1.19
0.84
2.18
1.04
1.31
0.61
1.61
0.00
1.98
Elii
den&s and most instars of Daphnia rosea.
As stated above, no feeding experiments
were done with C. americanus. However,
the two species which were used arc similar
to C. americanus, and they have elcctivity
functions that are similar to each other.
The feeding rate ( Table *6) and electivity
coefficients (Table 7) obtained for C. flavicans are substituted for C. americaws,
since thcsc species are most similar in size.
The density of fourth instar C. amSericanus larvae on representative
dates in
1968 can be found in Table 8.
The volume of Leechmere is about 1.36 X
lo7 liters. Thus, with the data from Tables
4, 6, and 8, we can estimate the Daphnia
per liter per day removed by the two
predators from the type A planktonic community of Leechmere (Table 9).
DISCUSSION
The distributions
of salamander and
midge larvae are strongly restricted by winter conditions.
Both live in ponds that
probably do not freeze solid in winter.
When a healthy population of salamanders
is feeding in such ponds that lack fish, one
finds a zooplankton community characterized by Chaobow
and a small species of
Daphnia, and no large Daphniu, large
copepods, or fairy shrimp. Furthermore,
the midge and small daphnid are only
found in ponds suppoarting either a salamander population or planktivorous
fish.
Because there is no evidence that the
TABLE 8.
The density of fourth instar Chaoborus
Date
Density
crustaceans are environmentally
limited in
their distribution in these alpine ponds, the
strong correlation of the distribution of the
various crustacean species with the prcsence of salamanders and midges suggests
a strong biological interaction.
The larval salamanders’ type of electivity
function favors the presence of the smaller
components of the zooplankton.
For example, during the transition from type B
to type A communities and early salamander larva dcvelopmcnt in Lcechmere, the
larger daphnid is proportionally
2 to 10
times as abundant in the salamanders’ diet
as in the plankton
(Table 3). Brooks
( 1968) reviewed evidence that this type of
size-selcctivc predation on the larger planktonic prey is the general vertebrate planktivore pattern,
The salamander is thus
responsible for the specific prey composition of the type A community.
It is just
these species that the midge may best USC
for food. Although
the correlation
betwcen midge and salamander distribution
is largely due to environmental
factors,
suitable midge food is scarcer in type B
communities, and therefore midge distribution may also be restricted by food requirements. More than half the size range of
each type B species (except D. cooiradensis) is greater than the largest food preferred by the midge, Therefore, in the
simple type A community, one predator
(the salamander) produces and maintains
a suitable feeding niche, via size-selective
( per liter )
americanus
larvae in Leechmere, 1968
25 Jun
9 Jul
19 Jul
29 Jul
13 Aug
28 Aug
12 Sep
0.06
0.01
0.01
0.27
0.45
0.65
0.27
136
STANLEY
TABLE 9. Comparative removal rates due to salamander and midge larvae predation, 1968
Daphnia
Date
25 Jun
9 Jul
19 Jul
29 Jul
13 Aug
28 Rug
12 Sep
_-._.
liter-l day-l removed by
___-______
salamander
Chaoborus
0.00038
0.048
0.061
0.085
0.060
0.016
0.014
0.19
0.03
0.03
0.86
1.44
2.08
0.87
Tota!
Da;~&-/
2.4
17.6
27.7
14.9
11.2
9.0
4.9
predation,
for a second predator
(the
midge larva ) . A priori, other dependent
predators, such as Diaptomus
shoshone
( Anderson 1967)) could co-octiur with the
salamander larvae. However, competition
between midge larvae and D. shoshone for
the few prey species is implied by similar
electivity
functions
(unpublished
data),
and salamander predation on the bright red
copepod must be relatively greater than on
the transparent midge larva. In more complex systems in large lakes, two or more
invertebrate
dependent predators do cooccur with size-selective vertebrate predators ( Tonolli 1962).
The electivity functions of the midge
and salamander larvae are complementary.
From the electivity functions (Tables 5 and
7) we see that the midge specializes on
daphnids
(and copepods) between the
lengths of 0.7 and 1.5 mm. Plankters above
about 1.7 mm are not caten. Conversely,
the salamander avoids plankters smaller
than about 1.0 mm and strongly selects
those over this length. Major food items
in the salamanders diet are planktonic amphipods 1,45 to 4.35 mm long and dipteran
larvae up to 12 mm long. The midge is
thus able to make use of a large portion of
the size distribution of the small zooplankters that are avoided by the salamander
larva. The midge’s preferred food size
range corresponds to the type A species size
ranges, while the salamander’s preferred
food is mo,re the size of type B plankters
or larger. The two electivity functions are
not complementary in the sense of shoting
equally strong food preferences. The salamanders may concentrate large zooplankters as much as 31 times over what is
I.
DODSON
available; the midges concentrate smaller
ones only as much as 2.8 times.
The salamander’s predation pattern determines the prey species with which it
coexists, but the salamander is not responsible for the major part of the mortality in
type A communities ( Table 9). In Leechmere, the total take of daphnids by salamander larvae was estimated to be about
a tenth that of the rather nonselective
midge larvae. (The salamander values may
be somewhat higher, since the estimates did
not include the average of 0.5 to 11 eggs
per female carried by the larger, adult
daphnids-the
size preferred by salamandcrs. ) Thus, the salamander larvae act as
a keystone species. Zooplankters are not a
major component of its diet, and salamanders prey relatively lightly on the zooplankton species. The few animals they do take
result in selection for the presence of small
species, and these are harvested by the
midge (for whom they arc a major part
of the diet),
There is much anecdotal evidence for
the widespread occurrence of complementary feeding niches in aquatic communities.
Galbraith’s (1967) study of the effect of
rainbow trout predation on lake zooplankton populations supports the complementary niche hypothesis. After rainbow trout
were added to Sporely Lake ( Michigan),
the relatively large D. pulex was replaced
by two smaller daphnid species and the
average daphnid size decreased from 1.4 to
0.8 mm. The standing crop of daphnids
decreased (but not the number of individuals) while that of other small cladoceran
species (Bosmina longirostris,
Chydorus
sphuericus, and Diaptomus minutes)
increased. Also Galbraith (personal communication)
found that the percentage of
daphnids between 0.4 and 0.7 mm increased from an average of 6% to 52% and
the daphnid predator Leptodora kindtii appeared after the addition of trout. Mordukhai-Boltovskaya
( 1958) showed that L.
kindtii does not eat cladocerans larger than
about 0.7 mm. Thus Leptodora appeared
in Sporely Lake only after the addition of
the size-selective predator, as if in response
SIZE-SELECTIVE PREDATION
to the increased food supply maintained
by the increased size-selective predation.
Along with the cladoceran predator Leptodora, species of Bythotrephes and Polypherr~u.s,the several species of large predatory
Calanoid copepods such as Limnocalunus,
Heterocope, and Epischura, and the numerous Chaoborus species all occur typically in the planktonic communities of large
lakes that generally contain one or more
strong size-selective predators (usually various species of planktivorous
fish).
[E.g.,
see the habitat preferences of these species
in Edmondson ( 1959 ) and Illics ( 1967). ]
Since these are all prey of size-selective
predators that feed using visual clues, it
is not surprising that they are morphologically similar. They are often quite attcnuate, about the same size (on the order of
0.5 to 1.5 cm long), and transparent or only
faintly colored. Where their food preferences have been investigated,
they are
known to prefer rotifers, the smaller spcties of Calanoid copepods, and clado&ra
less than 1.5 mm long, such as Ceriodaphnia spp. and Bosmina spp. (Berg 1937;
Mordukhai-Boltovskaya
1958). Thus, they
depend on the prey species whose presence
is favored by the highly selective feeding
behavior of the co-occurring predators.
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ANDERSON, R. S.
1967.
Diaptomid
copepods
from two mountain ponds in Alberta.
Can.
J. Zool. 45: 1043-1047.
137
1952.
Improvements
in the
interpretation
of recapture
data.
J. Animal
Ecol. 21: 120-127.
to the biology of
BERG, K. 1937. Contributions
Corethra
Meigen
( Chaoborus
Lichtenstein)
.
Biol. Medd. Danske Videnskab.
Selskab 13
(11):
l-101.
BROOKS,J. L. 1957. The systematics of North
Mem. Conn. Acad. Sci.
American Daphnia.
13. 180 p,
1968. The effects of prey size selcc-.
Syst. Zool. 17:
tion by lake planktivores.
272-291.
Predation,
AND S. I. DODSON. 1985.
Scibody size, and composition of plankton,
ence 150 : 28-35.
EDMONDSON, W. T. [ED.].
1959.
Fresh-water
biology, 2nd ed. Wiley.
1248 p.
GALDRAITH, M. G., JR. 1967. Size-selective predation on Daphnia by rainbow
trout and
yellow perch. Trans. Am. Fisheries Sot. 96:
l-10.
HRBBEEK, J. 1962
Species composition and the
amount of the zooplankton
in relation to the
fish stock. Rozpravy Cesk. Akad. Ved 10 ( 72 ) :
l-116.
ILLIES, J. 1967. Limnofauna Europaca.
Fischer.
474 p.
ecology of the
IVLEV, v. s. 1961. Experimental
Yale Univ. Press, New
feeding
of fishes.
IIaven, Conn. 302 p.
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