Empirical Relationships of Phytomacrofaunal Abundance to Plant
Biomass and Macrophyte Bed Characteristics1
Helene Cyr2 and John A. Downing
Departement de sciences biohgiques, University de Montreal, C.P. 6128, Succursale "A", Montreal (Quebec) H3C 3f7
Cyr, H., and J. A. Downing. 1988. Empirical relationships of phytomacrofaunal abundance to plant biomass and
macrophyte bed characteristics. Can. j. Fish. Aquat. Sci. 45: 975-984.
The abundance of phytophilous invertebrates was measured in 13 macrophyte beds and was related, using
multiple regression analysis, to the biomass of macrophytes among which the invertebrates were collected, the
average plant biomass growing per unit lake area, water and organic matter content of the sediments, total
phosphorus concentration in the water, rooting depth of the macrophyte bed, and sampling date. Quantitative
analyses are presented for chironomids, cladocerans, cyclopoid copepods, gastropods, water mites (Hydracarina),
ostracods, and trichopterans. R2 values for the regression equations ranged from 0.43 to 0.81. The abundance
of invertebrates was best related to the biomass of separate plant species, but equations based only on total plant
biomass sometimes had equivalent R2 values. In general, the abundance of phytophilous invertebrates was pos
itively related to areal plant biomass, sediment organic matter, and lake trophic status and negatively related to
depth. The abundance of phytophilous invertebrates generally rose throughout the sampling season. The sign of
the relationship with sediment water content, however, varied among invertebrate taxa. Macrophyte beds with
high areal plant biomass, in lakes with high total phosphorus concentration, support the greatest abundance of
potential invertebrate food for fish and waterfowl.
L'abondance des invert6br£s phytophiles a £t6 mesurSe dans treize lits de macrophytes; grace a une analyse par
regression multiple, l'abondance a e"t£ rapproch6e de la biomasse des macrophytes ou les invert6br6s ont ete
prelev6s, de la biomasse moyenne des plantes par unite" de surface lacustre, de la teneur en eau et en matieres
organiques des sediments, de la concentration en phosphore total dans I'eau, de la profondeur d'enracinement
du lit de macrophytes et de la date d'6chantillonnage. Des dosages ont 6t£ faits dans le cas des chironomid£s,
des cladoceres, des cope'podes cyclopidSs, des gastropodes, des hydrachnes (Hydracarina), des ostracodes et
des trichopterans. Les valeurs R2 obtenues gr£ce aux Equations de regression variaient entre 0,43 et 0,81. Les
meilleurs rapports ont £t§ obtenus entre les invert6br6s et la biomasse des especes v6g6tales conside>£es une a
une, mais les equations ou il n'&ait question que de la biomasse v6ge"tale totale avaient parfois des valeurs R2
gquivalentes. En ge'ne'ral, l'abondance des inverte"br6s phytophiles 6tait en correlation positive avec la biomasse
ve"g§tale du secteur consid£re, avec la teneur en matiere organique des sediments et avec le niveau trophique
du lac, mais en correlation negative avec la profondeur. G6ne>alement, on capturaitde plus en plus d'invert£br§s
phytophiles a mesure que la campagne d'6chantil tonnage progressait. Le fait que le rapport avec la teneur en
eau des sediments 6tait soit positif, soit nSgatif, dSpendait, cependant, des taxons d'invertebras considers. Les
lits de macrophytes a biomasse £lev£e dans les lacs a la concentration Slevee en phosphore total recelent la plus
grande abondance d'invertebre's qui peuvent servir a I'alimentation du poisson et de la sauvagine.
Received January 26, 1987
Accepted February 25, 1988
Requ le 26 Janvier 1987
Accepts le 25 fevrier 1988
(J9109)
The littoral zones of lakes sustain a highly diversified,
abundant, and productive invertebrate fauna, especially
when vegetated (Gerking 1964; Pieczynski 1977; Lim and
Fernando 1978; Gilinsky 1984). The phytophilic invertebrates
are very abundant, usually from 2 to 10 times more abundant
than littoral benthos (Pieczynski 1973; Soszka 1975; Vincent
et al. 1982), and could therefore play an important role in energy
transfer in lakes (Miura et al. 1978). Epiphytic invertebrates
represent an important source of food for juvenile and adult
fish (Mittelbach 1984; Keast 1985) and for waterfowl (Krull
■Publication No. 331 of the Groupe d'ecologie des eaux douces de
I'UniversitS de Montreal.
2Present address: Institute of Ecosystem Studies, Box AB, Millbrook, NY 12545, USA.
976
1970). The abundance of insect larvae in macrophyte beds is
also related to insect pest problems in lakeshore areas (Stimac
and Leong 1977). It would therefore be of theoretical and of
practical interest to predict the abundance of invertebrates in
macrophyte beds.
Despite their numerical importance, very little is known
about the distribution of epiphytic invertebrates, probably
because most work has been based on few, often qualitative
samples. Many studies are still based on qualitative sampling,
done by hand, with dip nets or with buckets (e.g. Gilinsky 1984;
Scheffer et al. 1984). More quantitative samplers are available
but many of these samplers yield inaccurate estimates of inver
tebrate abundance (Downing and Cyr 1985; Downing 1986).
Most published results are therefore biased. The problem is
Can. J. Fish. Aquat. Sci.. Vol. 45, 1988
worsened by the limited sampling on which most studies are
based, despite the notoriously high variability in invertebrate
abundance found within and among macrophyte beds (Mrachek
1966; Soszka 1975). In most studies, few replicate samples (n)
are collected within a macrophyte bed (e.g. Menzie 1980: n =
2; Crowder and Cooper 1982: n = 3; Dvorak and Best 1982:
n = 1; Vincent et al. 1982: n = 2; Rabe and Gibson 1984:
n = 1) and few macrophyte beds (h) are sampled (e.g. Mittelbach 1981,1984: h = 2 and 3, respectively; Biggs and Malthus 1982: h = 3; Cattaneo 1983: h = 1; Keast 1984: h = 3;
Rooke 1984, 1986a: s = 1 in both cases).
Most authors agree that the abundance of plant-dwelling
invertebrates in a macrophyte bed is related to the abundance
of aquatic plant species (Downing 1986), the physical and
chemical characteristics of the environment (Vincent et al.
1982), predation (Crowder and Cooper 1982), competition
(Paterson and Fernando 1971), or the emergence of insects (Stimac and Leong 1977). Although suggestive, these results are
either semiquantitative or are based on data from few sites and
lakes, and they have not yielded any model for predicting the
abundance of phytophilous invertebrates. We tested the
hypotheses that the abundance of invertebrates in different
macrophyte beds is related to (1) the biomass of macrophytes
and (2) macrophyte bed characteristics, including plant density,
sediment quality, lake trophic status, and rooting depth. The
abundance of phytophilous invertebrates is usually positively
related to plant density (Macan and Kitching 1972; Crowder
and Cooper 1982). Dense macrophyte beds could, for example,
reduce fish predation (Crowder and Cooper 1982), increase total
periphyton biomass by providing more colonizable substrate
(Kowalczewski and Pieczynska 1976), increase silt sedimen
tation favorable to detritus feeders (Petr 1968), and reduce wave
action detrimental to loosely attached epiphytic invertebrates
(Dejoux and Saint-Jean 1972). Sediment quality has also been
suggested to influence the distribution of benthic invertebrates
(Cole and Weigmann 1983; Vodopich and Cowell 1984). It
might therefore be related to the distribution of epiphytic inver
tebrates which overwinter in the sediments and colonize the
plants again in summer (Menzie 1980; Cattaneo 1983). We also
expect a positive relationship between the abundance of plantdwelling invertebrates and the concentration of total phospho
rus in the water, suggested by the relationship found between
total phosphorus concentration and the biomass of epiphytic
and planktonic algae on which epiphytic invertebrates feed
(Cattaneo and Kalff 1980; Downing 1981; McQueen et al.
1986).
L MEMPKREMAGOG
m
COVE ISLAND
BAY
Fig. 1. Location of the sampling sites.
Can. J. Fish. Aquat. Sci., Vol. 45, 1988
911
Table 1. Characteristics of the 13 sampling sites. The average measures of areal plant biomass (PBA),
proportion by weight of sediment water content (SWC) and organic matter content (SOC), total phos
phorus concentration in the water around the macrophyte bed (TP), and rooting depth of the macrophyte
bed (Z) are presented for each site, with their standard deviations in parentheses. Macrophyte species
composition includes all plant species, listed in decreasing order of importance, that represented more
than 1% of the total macrophyte biomass: C, Chara sp.; CC, Cabomba caroliniana; CD, Ceratophyllum
demersum; EC, Elodea canadensis; I, Isoetes sp.; J, Juncus sp.; M, Myriophyllum spicatum and M.
humile in Lake Des lies; NF, Najasflexilis; NH, Nitella hyalina; P, Potamogeton sp.; PA, Potamogeton
amplifolius; PE, a mixture of Potamogeton epihydrus and P. gramineus; PR, Potamogeton robbinsii',
S, Sagittaria sp.; U, Utricularia sp.; VA, Vallisneria americana. The sampling day is a numerical date
ranging from day 1 (July 3, 1984) to day 55 (August 26, 1984).
PBA
Lake
Brome
(Eagle Island)
Champlain
(Baie de Venise)
Champlain
(Kings Bay)
Des lies
Echo
Fournelle
Ludger
(g/m2)
Memphremagog
(Sargent's Bay)
Memphre'magog
(Three Sisters
(Cove Island Bay)
Quenouilles
(m)
16
1.7
(2)
(0.2)
32
(8)
0.25
(0.06)
0.36
0.014
12
(0.005)
0.021
(2)
(0.1)
7
2.2
(88)
(0.02)
(0.003)
(2)
(0.2)
0.48
0.013
(0.003)
0.014
11
(1)
(0.01)
8
2.0
(0.003)
0.033
(0.004)
0.020
(0.008)
0.026
(0.004)
0.035
(0.008)
0.022
(0.00003)
(2)
(0.2)
12
1.9
(0.2)
63
(120)
256
(116)
40
131
397
(428)
85
(86)
48
(80)
(0.03)
0.96
(0.01)
0.48
(0.02)
0.28
(0.06)
0.40
(0.04)
0.60
(0.10)
0.32
(0.03)
—
(4)
1.4
2.7
(7)
(0.2)
12
2.0
(0.6)
3.0
(0.4)
(2)
7
(1)
0.007
12
1.4
(4)
(0.1)
182
(108)
0.46
(0.02)
0.027
10
1.6
(0.004)
(2)
(0.00)
At each site, 15-20 samples of plant-dwelling invertebrates
were collected by gentle closure of a 6-L plastic box (Downing
1986) over plants. The samples were distributed at random
points along either side of a SO-m transect positioned parallel
to shore. Each sample was also taken at a randomly chosen
VA, PR, M,
54
PA, EC
M, PR,
I, S
PA
55
12
PR, PA, EC
7
PA, J, U,
C, NH, PR
27
40
CD, P
(0.002)
Phytomacrofauna Samples
42
PR, EC, M,
0.19
bed, and the sampling date. The sampling date was included
as a covariable in the analysis to compensate for seasonal trends
in invertebrate abundance.
VA, M, P
1.4
(0.02)
which they were found, the characteristics of the macrophyte
34
(0.04)
28
Sampling
day
VA.EC
38
76
Thirteen macrophyte beds of mixed plant species were sam
pled from 10 lakes within a 150-km radius of Montreal, Quebec
(45°31'N, 73°36'W), during July and August 1984 (Fig. 1;
Table 1). Macrophyte beds larger than 100 m2 were sought at
sites differing in trophic status and depth and were selected to
vary in plant density and species composition. The abundance
of phytophilous invertebrates was estimated at each site and
related, by regression analysis, to the biomass of plants among
Macrophyte
species
composition
(12)
(30)
Methods
978
(jAg/U
1.8
(0.2)
3.1
—
Island)
Memphremagog
Z
(88)
276
(177)
65
(108)
Massawippi
(Ayer's Cliff)
SOC
9
(17)
88
(84)
Magog
SWC
TP
M
14
P, M, VA
M, PR, VA,
1
48
PE, EC
P, VA, CC,
NH, EC,
NF
PR
21
28
height along the plant stems to estimate the average abundance
of invertebrates, regardless of their vertical distribution. We
included a wide range of macrophyte abundance and macro
phyte species composition into the samples to maximize the
range of applicability of our regression equations.
The volume of each phytomacrofauna sample was reduced
by filtration through a 100-|xm Nitex-mesh filter funnel (Likens
and Gilbert 1970) and the samples were kept cold during trans
port to the laboratory. The invertebrates retained on the
100-|im filter were then carefully washed from the macrophytes
and preserved in 80% ethanol (with 1% glycerine to prevent
desiccation; Cyr 1986). The macrophytes were separated by
species (Fassett 1957), dried at 60°C to constant weight, and
weighed (±0.1 mg). All invertebrates in 231 samples were
counted at 16 x magnification and separated into major taxonomic groups. We collected amphipods, cladocerans, copepods, flatworms (Turbellaria), gastropods, insect larvae, isopods, leeches, nematodes, ostracods, tardigrades, and water
mites (Hydracarina). Oligochaetes were often found broken in
the samples and were therefore not counted. The abundance of
oligochaetes varied among sites and their omission underesti
mates, although not in a systematic fashion, the total counts of
Can. J. Fish. Aquat. ScL, Vol. 45, 1988
invertebrates. The phytomacrofauna samples provided data on
the abundance of invertebrates and on the biomass of plants
supporting them.
Macrophyte Bed Characteristics
In each macrophyte bed, we measured the biomass of macrophytes per unit lake area, some sediment characteristics, the
total phosphorus concentration of the water surrounding the
plants, and the depth at the site. At each site, 25 quadrat sam
ples of plants (112 cm2; Downing and Anderson 1985) were
randomly collected along the 50-m transect used for phytomacrofaunal sampling. The macrophytes were separated by
species, dried at 60°C to constant weight and weighed
(±0.1 mg). A sediment sample was taken by a diver at the
center of each harvested quadrat, using a 5.6-cm-diameter
handcorer. The overlying water in the core tube was gently
poured out and the top 10 cm of sediments isolated for analysis.
The sediments were homogenized and the percentage water and
organic matter content measured. The sediment water content
was calculated as (WW - DW)/WW where WW is sediment
wet weight and DW is the weight of sediments dried at 60°C
to constant weight. The sediment organic matter content was
estimated as the ash-free dry weight and calculated as (DW AW)/DW where AW is ash weight from sediments burned at
550°C to constant weight. Water samples for total phosphorus
analyses were collected 15-30 cm below the lake surface at 10m intervals along the 50-m transect. Phosphorus analyses were
performed by persulfate digestion, followed by the ascorbic acid
colorimetric method (American Public Health Association et
al. 1985) with readings taken after 45-60 min. Water depth in
the macrophyte bed was also measured (± 0.1 m) at 10-m inter
vals along the transect. Average measures of macrophyte bio
mass per unit lake area (25 samples), sediment water and
organic matter content (25 samples), total phosphorus concen
tration of the water (6 samples), and rooting depth of the macro
phyte bed (6 measures) were calculated and macrophyte species
composition was noted at each site (Table 1). Sampling dates
were entered in the regressions using a day number ranging
from day 1 (July 3,1984) to day 55 (August 26,1984) (Table 1).
Statistical Analysis
The relationships between the abundance of invertebrates,
the biomass of macrophytes, macrophyte bed characteristics,
and sampling date were quantified using forward stepwise lin
ear multiple regression analysis. Separate analyses were per
formed for each of the common taxonomic groups encountered
and for the total of all invertebrates.
The variables used in our analyses were transformed to nor
malize the residuals and equalize their variances. We trans
formed the abundance of chironomids, cyclopoids, water mites,
ostracods, and the total abundance of invertebrates to their
fourth root ((Y)°■2S), the abundance of cladocerans to logarithms
(log(10), the abundance of Bosmina longirostris, Camptocercus
sp., Chydorus sphaericus, Eurycercus lamellatus, Sididae,
gastropods, and trichopterans to log(F + 1), the abundance of
other chydorid cladocerans to log(l/(y + 1)), and the biomass
of plant species to either fourth root ((X)°2S) or to logarithm
(log(X + 0.0001)). Arc-sine transformations for percentages
(Draper and Smith 1981, p. 239) were attempted on the ratios
of water and organic matter in the sediments, but did not
improve the fit of the regression or the distribution of the resid
Can. J. Fish. Aquat. Set, Vol. 45, 1988
uals. Data on the five environmental variables and sampling
day were left untransformed.
Two series of regressions were performed: (A) including the
total biomass of macrophytes collected in the phytomacrofauna
samples and (B) including the biomass of each macrophyte spe
cies collected in the phytomacrofauna samples. For each inver
tebrate taxon, we obtained two equations of the form
Y, = bxXx + bj(2 + ... + bJCk + a
where K, is the transformed abundance of invertebrates from
taxon i, Xx toXk are transformed macrophyte biomass collected
in the phytomacrofauna samples (either total in equations of
type A or separated by species in equations of type B), envi
ronmental variables and sampling day, bx to bk are fitted coef
ficients, and a is the stochastic error term. Only variables with
regression coefficients significantly different from zero (P(f) <
0.05) were retained in the equations. We obtained equations
relating the abundance of each invertebrate taxon to the biomass
of plants among which they were collected, macrophyte bed
characteristics, and sampling date. Significance of the regres
sion coefficients b{ to bk was taken as validation of the rela
tionship between the abundance of epiphytic invertebrates, the
biomass of macrophytes, and macrophyte bed characteristics.
Results and Discussion
Both hypotheses were upheld. The regression coefficients for
macrophyte biomass and macrophyte bed characteristics were
often highly significant. The abundance of phytophilous inver
tebrates was therefore related to biological, physical, and chem
ical characteristics of the habitat and varied in a consistent way
throughout the sampling period. Multivariate relationships were
fitted for the total abundance of invertebrates, the total abun
dance of cladocerans, and the abundance of 12 other inverte
brate taxa (Tables 2 and 3). All equations were highly signifi
cant (P(F) < 0.0001) and explained 43-81% of the variance in
transformed invertebrate abundance.
In most cases, transformations permitted valid analyses to be
performed. Unfortunately, the equations for the cladocerans B.
longirostris, E. lamellatus, the gastropods, and the trichopter
ans had heteroscedastic residuals even after transformation of
the dependent and independent variables (Cyr 1986). In all
cases, the heteroscedasticity of the residuals resulted in an overestimation of both the overall regression F-values and the tvalues for each regression coefficient (Gujarati 1978, p. 199).
Too many significant F- and f-values were therefore found (type
1 error). Given the high significance of these equations (P(F)
< 0.0001; Tables 2 and 3) and of their regression coefficients,
however, the results are probably robust to such departures from
the homoscedasticity assumptions.
We could not fit equations with unbiased, normal, and homoscedastic residuals for invertebrate taxa that were rare or absent
in several lakes, namely amphipods, cladocerans such as
Daphnidae (including Ceriodaphnia sp., Daphnia sp., Simocephalus sp.), llyocryptus sp., Macrothrix sp., Ophryoxus sp.,
and Polyphemus sp., calanoid and harpacticoid copepods,
Hirudinea, insects belonging to the orders Coleoptera, Diptera
(Ceratopogonidae and Tipulidae), Ephemeroptera, Lepidoptera, Megaloptera, and Odonata, isopods, nematodes, tardigrades, and turbellarians. The abundance of the most common
taxa, however, was strongly related to the biomass of macro
phytes, environmental characteristics, and sampling day.
979
Table 2. Multivariate equations relating the abundance of phytophilous invertebrates to total plant biomass collected in phytomacrofaunal samples
(BPL), macrophyte bed characteristics, and sampling date (SD). All equations are highly significant (P(F) < 0.0001). The adjusted R2, the Fvalue, and the effective (n) are presented for each equation. Invertebrate taxa: CHIR, chironomids; CLAD, total cladocerans; BOSM, Bosmina
longirostris; CAMP, Camptocercus sp.; CHYD, Chydorus sphaericus; ALON, other Chydorinae; EURY, Eurycercus lamellatus; SIDA, Sididae;
CYCL, cyclopoids; GAST, gastropods; ACAR, water mites (Hydracarina); OSTR, ostracods; TRIC, trichopterans; TOTAL, all invertebrates
retained on a 100-[x filter, excluding the oligochaetes. The abbreviations for macrophyte bed characteristics are as in Table 1.
Adjusted
R2
Equation
(CHIR)025 = 3.2(BPL)O25 + 0.004 PBA + 0.03 TP - 1.0 Z + 0.01 SD + 1.5
log(CLAD) = 0.49 log(BPL) + 0.002 PBA - 0.5 SWC + 47 SOC - 0.7 Z + 0.009 SD + 2.9
log(BOSM) = -0.21 log(BPL) + 0.009PBA - 1.4 SWC + 97 SOC - 0.08 TP - 1.6 Z + 0.03 SD + 1.8
log(CAMP) = 0.73 log(BPL) - 0.002 PBA + 0.04 TP + 0.6 Z - 0.01 SD + 0.38
log(CHYD) = 0.29 BPL + 0.9 SWC + 65 SOC + 0.03 TP - 0.8 Z + 0.03 SD - 0.1
log(l/(ALON)) = -0.55 log(BPL) - 0.003 PBA - 1.7 SWC - 38 SOC + 0.6 Z - 0.03 SD - 0.1
log(EURY) = 0.20 BPL - 1.6 SWC + 40 SOC + 0.03 TP + 0.6 Z - 0.04 SD - 0.2
log(SIDA) = 0.25 log(BPL) + 0.001 PBA - 2.1 SWC - 0.5 Z - 0.02 SD + 3.5
(CYCL)023 = 2.1 (BPL)025 + 0.001 PBA + 50 SOC + 0.02 TP + 0.3
log(GAST) = 0.46 BPL - 0.006 PBA - 0.8 SWC - 40 SOC + 0.03 TP + 0.8 Z - 0.02 SD + 1.1
(ACAR)025 = 2.7 (BPL)025 - 0.01 TP - 0.8 Z + 0.02 SD + 1.3
(OSTR)025 = 2.3 (BPL)025 - 0.004 PBA + 0.09 TP + 0.8 Z + 0.02 SD - 1.3
log(TRIC) = 0.33 BPL - 7 SOC + 0.02 TP + 0.009 SD + 0.1
(TOTAL)0 25 = 4.3 (BPL)025 + 0.002 PBA + 58 SOC + 0.04 TP - 0.9 Z + 0.03 SD + 1.3
F
0.62
76
0.68
0.75
0.43
0.63
68
193
87
199
231
0.49
0.76
0.57
0.50
36
56
33
106
54
50
0.56
38
0.43
0.56
0.43
0.61
44
58
38
49
231
198
197
199
198
199
199
229
224
197
186
Table 3. Multivariate equations relating the abundance of phytophilous invertebrates to the biomass of plant species, macrophyte bed charac
teristics, and sampling date (SD). All equations are highly significant (P(F) < 0.0001). The adjusted R2, the F-value, and the effective (n) are
presented for each equation. The abbreviations for invertebrate taxa are as in Table 2; plant species and macrophyte bed characteristics are as
in Table 1.
Adjusted
Equation
R2
(CHIR)025 = 2.3 (J)025 + 1.8 (PA)025 + 1.7 (PR)025 + 1.7 (M)025 + 1.2 (CD)025
+ 0.7 (VA)025 + 0.005 PBA + 0.04 TP - 1.1 Z + 0.01 SD + 2.9
0.59
34
231
log(CLAD) = 0.49 M + 0.48 P + 0.39 PA + 0.15 PR + 0.002 PBA + 41 SOC - 0.8 Z
0.70
58
193
0.79
75
199
0.56
0.66
59
231
45
198
0.62
32
197
0.81
145
199
0.60
34
198
0.51
30
199
0.63
29
199
0.51
34
229
(OSTR)025 =2.5 (CD)025 + 2.1 (VA)025 + 1.6 (PR)025 + 1.6 (U)025 + 1.4 (EC)025
+ 1.2 (M)025 + 0.8 (PA)025 + 0.8 (P)025 - 0.005 PBA + 0.1 TP + 1.1 Z - 0.6
0.70
47
224
log(TRIC) = 16.0 NH + 1.1 CC + 0.8 CD + 0.7 PA + 0.4 PR + 0.2 M + 0.0007 PBA
0.52
24
197
0.59
27
186
+ 0.02 SD + 2.3
log(BOSM) = -0.191og(CD) - 0.191og(VA) - 0.08 log(M) - 0.06 log(PR) + 0.009 PBA
- 2.0 SWC + 89 SOC - 0.09 TP - 1.4 Z + 0.03 SD + 0.3
log(CAMP) = 0.23 log(PA) + 0.16 log(M) - 0.14 log(VA) + 0.03 TP + 0.2 Z + 1.2
log(CHYD) = 1.3 CC + 1.3 CD + 0.5 M + 0.3 VA + 1.5 SWC + 60 SOC + 0.2 TP - 1.0 Z
+ 0.04 SD + 0.1
log(l/(ALON)) = 0.17 log(VA) - 0.13 log(M) - 0.20 log(U) - 0.24 log(PA) - 0.005 PBA
- 1.3 SWC - 31 SOC + 0.02 TP + 0.8 Z - 0.03 SD - 1.8
log(EURY) = 0.54 M - 1.1 SWC + 30 SOC + 0.03 TP + 0.4 Z - 0.03 SD + 0.1
log(SIDA) = 0.22 log(NH) + 0.08 log(PA) - 0.13 Iog(U) - 0.14 log(PR) + 0.003 PBA
- 1.3 SWC + 20 SOC - 0.02 TP - 0.9 Z + 3.2
(CYCL)025 = 1.4 (M)025 + 1.3 (PA)025 + 0.6 (PR)025 + 0.004 PBA + 50 SOC - 0.5 Z
+ 0.009 SD + 2.0
log(GAST) = 8.2 J + 1.0 P + 1.0 PA + 0.5 PR + 0.3 VA + 0.3 M - 0.006 PBA - 0.9 SWC
- 37 SOC + 0.04 TP + 1.0 Z - 0.02 SD + 0.6
(ACAR)025 = 2.0 (PR)025 + 1.8 (PA)025 + 1.0 (CD)025 + 0.6 (VA)025 + 0.5 (M)025
- 0.002 PBA + 0.03 TP + 1.3
+ 0.02 TP + 0.01 SD - 0.3
(TOTAL)025 = 3.2 (M)025 + 2.5 (PA)025 + 2.4 (U)025 + 2.0 (CD)023 + 1.9 (PR)025
+ 1.4 (VA)025 + 0.006 PBA + 52 SOC - 1.9 Z + 0.04 SD + 4.5
Macrophyte Biomass in the Phytomacrofaunal Samples
The abundance of phytophilic invertebrates was in general
positively related to macrophyte abundance (Table 4), corrobo
rating the suggestions of Gerking (1957) and Krull (1970). The
only exception is the cladoceran B. longirostris which was neg
atively related to the biomass of macrophytes (Table 4). Bos
mina longirostris are found both among macrophytes and in
980
open water (Pennak 1966; Gliwicz and Rybak 1976). Within
macrophyte beds, however, we found more B. longirostris when
fewer plants were collected, suggesting that they were more
abundant in the water around the plants than directly on the
plants. The abundance of the eurytopic C. sphaericus (Pennak
1966; Lim and Fernando 1978), on the other hand, was posi
tively related to the biomass of macrophytes (Table 4). When
undisturbed, C. sphaericus, like other chydorids, spends most
Can. J. Fish. Aquat. Sci., Vol. 45. 1988
Table 4. Signs of regression coefficients associated to total plant biomass collected in the phytomacrofaunal samples (BPL) in the equations of type A (Table 2) and to the biomass of each plant species
in the equations of type B (Table 3). Partial /-"-values, a measure of the variation in invertebrate abun
dance explained by each variable, are given in parentheses; "ns" indicates that the regression coefficient
is not significantly different from zero (P(t) > 0.05); symbols for the species of macrophytes are as in
Table 1.
TypeB
Dependent
Type A
variable
BPL
CC
CD
EC
J
M
NH
P
+
ns
+
ns
+
+
ns
ns
Chironomidae
(166)
Cladocera
+
(12)
(7)
ns
ns
ns
ns
ns
—
ns
ns
(77)
Bosmina
longirostris
Camptocercus sp.
—
(14)
+
(26)
+
ns
ns
ns
ns
Sididae
+
+
+
ns
ns
(4)
(9)
—
+
ns
ns
ns
ns
ns
ns
ns
ns
+
+
+
+
ns
ns
ns
+
ns
+
ns
ns
ns
ns
ns
ns
ns
+
(75)
Total
+
(169)
+
(10)
ns
+
ns
ns
(8)
ns
(54)
Trichoptera
ns
ns
+
ns
+
ns
ns
(67)
+
(9)
(9)
ns
+
+
—
(30)
ns
ns
(79)
(36)
ns
ns
ns
ns
ns
ns
ns
+
ns
+
ns
ns
+
ns
+
(7)
(68)
ns
ns
+
ns
+
(7)
ns
ns
ns
(19)
+
+
+
(24)
+
ns
ns
+
+
(13)
ns
(6)
(18)
ns
ns
ns
—
—
ns
ns
+
(21)
ns
(13)
ns
+
(140)
+
(79)
+
(38)
+
ns
+
(8)
+
ns
(4)
ns
+
(16)
+
(58)
ns
+
(87)
ns
(5)
ns
ns
(11)
+
ns
(50)
+
+
(55)
+
+
(12)
ns
(113) (157)
(30)
(8)
+
(47)
(14)
(32)
+
+
+
(14)
(63)
(145)
Ostracoda
VA
(5)
(6)
(88)
Hydracarina
ns
U
(79)
(66)
Gastropoda
(18)
ns
(15)
(15)
Cyclopoida
(5)
ns
+
PR
(41)
(20)
+
+
(45)
(39)
Eurycercus
lamellatus
ns
(10)
(76)
Chydorus
sphaericus
Other Chydorinae8
+
+
(82)
(99)
(8)
+
(66)
PA
+
+
(11)
+
(5)
(73)
ns
ns
(66)
+
(57)
+
+
(6)
(16)
"The signs of regression coefficients in the equation for the transformed abundance of Chydorinae
(log(l/(K + 1)) were inverted to facilitate comparison with other invertebrate taxa.
of its time attached to solid surfaces (Fryer 1968). Chydorus
sphaericus is perhaps more dependent on submerged plants, at
least for support, than is B. longirostris. Eurycercus lamellatus
is a weed-frequenting cladoceran that is commonly found on
Myriophyllum spicatum (Fryer 1963; Flossner 1964). Its abun
dance in our samples was also strongly related to the biomass
ofMyriophyllum spp. (Table 4) which alone accounted for 54%
of its variance. Sida crystallina is usually found attached to
broad-leaved plants, especially Potamogeton (Smyly 1952; Entz
1947). The abundance of Sididae, composed mostly of 5. crys
tallina and of some Diaphanosoma sp., was positively related
to the biomass of the broad-leaved Potamogeton amplifolius but
also to the filamentous macroalgaMte//a hyalina and was neg
atively related to the biomass of the narrower Potamogeton robbinsii and of the delicate Utricularia sp. (Table 4). The abun
dance of other taxa and of total invertebrates was positively
related to plant biomass.
Some invertebrate groups seem to colonize various plant spe
cies preferentially, while others seem to be equally attracted to
any plant substrate. Comparison of the adjusted R2 values of
the equations including total plant biomass (type A) and the
biomass of separate plant species (type B) shows that the abun
dance of gastropods, water mites (Hydracarina), ostracods, and
trichopterans was best related (highest R2) to the biomass of
Can. J. Fish. Aqua!. Sci., Vol. 45, 1988
particular plant species. These equations explained between 7
and 13% more variation in invertebrate abundance than the
equations including only total plant biomass (Tables 2 and 3).
This supports the general belief that epiphytic invertebrates are
related differently to plant species (Andrews and Hasler 1943;
Soszka 1975; Gerrish and Bristow 1979; Rooke 1986b). On the
other hand, the abundance of chironomids, most cladoceran
taxa, and cyclopoid copepods was related equally well (AR2 <
0.05) to the biomass of separate plant species and total plant
biomass (Tables 2 and 3). Detailed comparisons of the abun
dance of epiphytic invertebrates among different plant species
are presented elsewhere (Cyr 1986).
Environmental Variables
Biological, physical, and chemical characteristics of the
macrophyte bed environment also accounted for variability in
the abundance of phytomacroinvertebrates, as suggested by
many authors (Stimac and Leong 1977; Vincent et al. 1982;
Scheffer et al. 1984).
The abundance of most invertebrate taxa was positively
related to the average biomass of plants growing per unit lake
area (Table 5). Cladocerans were most abundant in macrophyte
beds with high areal plant biomass, corroborating the qualita981
Table 5. Signs of regression coefficients (+ and -) associated to
macrophyte bed characteristics and sampling day (SD) in the equations
of type B (Table 3). The symbols and partial F-values (in parentheses)
are as in Table 1. "ns" indicates a regression coefficient that is not
significantly different from zero (P > 0.05); a dash (—) indicates that
the variables were not included in the analysis.
Dependent
PBA
variable
(g/m2)
Chironomidae
SWC
SOC
+
+
longirostris
Camptocercus sp.
SD
_
+
(17)
ns
(68)
Bosmina
Z
(m)
+
(29)
Cladocera
TP
(u-g/L)
+
ns
sphaericus
Other Chydorinae1
(219)
(149)
—
+
—
—
(271)
(57)
(335)
(218)
(135)
ns
—
—
+
+
ns
+
(77)
Eurycercus
lamellatus
Sididae
ns
+
+
(39)
(141)
+
(19)
-
(32)
+
(70)
Cyclopoida
+
—
(49)
ns
Hydracarina
Ostracoda
+
(30)
+
(66)
+
(24)
+
-
-
(116)
(14)
-
—
-
(56)
—
Total
(56)
+
(57)
—
(12)
ns
+
(44)
+
(85)
+
(65)
ns
(9)
-
+
(155)
(117)
-
(38)
+
(41)
—
+
(92)
-
(149)
ns
(165)
-
(17)
(151)
ns
ns
+
(84)
+
(5)
-
(32)
ns
ns
+
ns
+
(49)
ns
(60)
(7)
+
(6)
+
-
+
-
(7)
+
(30)
(21)
(66)
Trichoptera
+
(27)
(46)
(50)
Gastropoda
—
+
(58)
Chydorus
(34)
ns
+
(20)
ns
+
(65)
—
(110)
+
(56)
'The signs of regression coefficients in the equation for the trans
formed abundance of Chydorinae (log(l/(F +1)) were inverted to
facilitate comparison with other invertebrate taxa.
tive observations of Smyly (1952). The abundance of Sididae,
chironomids, and trichopterans was also positively related to
areal plant biomass. These invertebrate taxa are important prey
of littoral fish (Gerking 1962; Fairchild 1982), and their large
abundance in dense macrophyte beds could therefore result from
reduced fish predation (Crowder and Cooper 1982). High areal
plant biomass, on the other hand, supported few gastropods
(Table 5), contrary to the expectation of 0kland (1983).
The abundance of many taxa of plant-dwelling invertebrates
was also related to sediment quality (Table 5). Sediment water
and organic matter content were strongly related to the abun
dance of most cladoceran groups (P < 0.0001; Table 5),
corroborating the qualitative observations of Smyly (1952).
Sediment characteristics are indeed likely to influence at least
the distribution of chydorid cladocerans which are found both
among the vegetation and in the sediments (Fryer 1963, 1968).
The abundance of gastropods was negatively related to sedi
ment water content, possibly from the lack of support offered
by fluid sediments (0kland 1983). The effect of sediment water
content varied among invertebrate taxa, while the organic mat
ter content was mostly positively related to invertebrate
abundance.
The abundance of most invertebrate taxa was positively
related to total phosphorus levels in the water (Table 5). This
is not surprising, since the biomass of epiphytic and planktonic
982
algae, on which the invertebrates feed (Downing 1981; Cattaneo 1983), is also positively related to the total phosphorus
concentration in the water column (Cattaneo and Kalff 1980;
McQueen et al. 1986). The abundance of B. longirostris, Chy
dorinae (excluding Camptocercus sp. and C. sphaericus), and
Sididae, however, was negatively related to total phosphorus
concentrations (P < 0.05; Table 5). Young (1945) and Quade
(1969) also found 5. crystalline mostly in clear littoral zones
with low periphyton biomass. This is possibly due to the inhib
itory effect of high seston concentration on the feeding of S.
crystalline (Downing 1981). In general, more epiphytic inver
tebrates were found in eutrophic lakes.
Depth has a significant influence on the abundance of most
taxa of plant-dwelling invertebrates. We sampled macrophyte
beds growing between depths of 1.4 and 3.1m. The total abun
dance of epiphytic invertebrates was negatively related to depth
(P < 0.0001; Table 5), corroborating the observations of
Soszka (1975). Various invertebrate taxa, however, responded
differently to depth. The abundance of gastropods was posi
tively related to depth (P < 0.0001; Table 5), contrary to the
observations of Stariczykowska (1960), who found no differ
ence in gastropod abundance on either of five plant species
between shallow and deep (about 5 m) portions of the littoral
zone. Chironomids, on the other hand, were negatively related
to depth (P < 0.001; Table 5), a result which is consistent with
the observations of Entz (1947) and Vodopich and Cowell (1984,
benthic Procladius culciformis) but different from those of
Soszka (1975). Cladocerans and cyclopoid copepods were also
more abundant in shallow macrophyte beds (Table 5).
Seasonal Effect
We sampled all macrophyte beds in the shortest time possible
to minimize seasonal variability in invertebrate abundance
among sampling sites. Sampling each macrophyte bed took
about 130 person-hours of laboratory and field work (see also
Downing and Cyr 1985) and sampling trips were spaced as
closely as possible. All phytomacrofauna samples were col
lected during July and August, excluding the fall period where
the largest increase in invertebrate abundance is usually
observed (Smock and Stoneburner 1980; Rooke 1986a). Despite
these precautions, the abundance of most invertebrate taxa in
our samples increased systematically through the summer (P <
0.05; Table 5), as suggested by Mrachek (1966), Soszka (1975),
Keast (1985), and Rooke (1986a). The introduction of sampling
date in the multivariate equations helped explain up to 25%
more variance in invertebrate abundance among samples (Cyr
1986, appendix F). Total invertebrate abundance and the abun
dance of chironomids, cladocerans, cyclopoid copepods, and
trichopterans increased through the summer (P < 0.05;
Table 5). Our results differ from those of Mrachek (1966) who
found, within a lake, a decrease in the abundance of chiron
omids and no variation in trichopteran numbers throughout the
season. The abundance of gastropods per unit plant biomass,
on the other hand, decreased from July to August (P < 0.0001;
Table 5). Plant biomass therefore increases faster than the
abundance of gastropods, as suggested by Pip and Stewart
(1976), but slower than the abundance of most other inverte
brate taxa.
Potentially Advantageous Macrophyte Beds for Fish and
Waterfowl
Before our equations can be used for the prediction of phytomacrofaunal abundance, they should be validated using indeCan. J. Fish. Aquat. Sci., Vol. 45. 1988
pendent observations (Berk 1984). Unfortunately, this is impos
sible, since so few quantitative data have been published on the
abundance of epiphytic invertebrates. Our results, however, can
be summarized for practical use in fishery and waterfowl man
agement. These results must be used carefully, since the acces
sibility of invertebrates also influences their availability as food
for fish and waterfowl (Crowder and Cooper 1982; Gilinsky
1984). Large cladocerans (E. lamellatus, S. crystallina), gas
tropods, and insect larvae are the most important food source
for fish (Gerking 1962; Fryer 1963; Fairchild 1983; Mittelbach
1984). Macrophyte beds supporting large abundances of these
invertebrates could potentially be the most important for fish
eries. Our sampling sites ranged from low plant biomass per
unit lake area to biomasses greater than the world average (310
g/m2; Duarte et al. 1986), had a wide range of sediment water
content, generally low organic matter content, and were located
in oligomesotrophic to eutrophic waters, depths of 1.4-3.1 m.
Macrophyte beds with high plant biomass per unit lake area,
covering sediments of low water content in eutrophic lakes,
yielded the highest abundances of fish food organisms per unit
macrophyte biomass (Table 5). Crowder and Cooper (1982),
however, found that the feeding efficiency of fish decreased
with increasing plant density and that fish grew best at inter
mediate plant density. Within the range of our sampling sites,
sediment organic matter content and depth did not affect the
abundance of fish food invertebrate taxa in any consistent way.
Waterfowl feed mostly on amphipods and aquatic insect larvae
(Moyle 1961; Danell and Sjoberg 1980). We found no consis
tent pattern in the distribution of amphipods, which were only
rare components of the phytomacrofauna in 10 of our 13 sites.
The abundance of chironomid and trichopteran larvae per unit
plant biomass, however, was higher in macrophyte beds with
high areal plant biomass located in shallow macrophyte beds in
waters of high total phosphorus concentration (Table 5).
Because the size of macrophyte beds is the prime determinant
of the total abundance of phytophilous invertebrates in lakes
(Smirnov 1963; Glowacka et al. 1976), general enhancement
of macrophyte abundance could lead to increased fish (Durocher et al. 1984) and waterfowl abundance. This research has
shown, however, that macrophyte species composition, macro
phyte standing stock, sediment characteristics, total phospho
rus concentration in the water around the plants, rooting depth
of the macrophyte bed, and sampling date are also strongly
related to the total abundance of phytomacroinvertebrates and
to the abundance of individual invertebrate taxa. The abun
dance of invertebrates in the littoral zones of lakes is a multi-
variate correlate of many characteristics of the littoral habitat.
Acknowledgments
We thank D. Miron and Y. Rochon for patient field work and A.
Cattaneo, B. Pinel-Alloul, N. C. Collins, and an anonymous reviewer
for comments on the manuscript. We gratefully acknowledge the finan
cial support of the Canadian National Sportsmen's Fund, the Natural
Sciences and Engineering Research Council of Canada, the Minister
of Education of the Province of Quebec (FCAR), and Outboard Marine
Corp. of Canada, Ltd.
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