Limnol. Oceanogr., 41(2), 1996,243-252
0 1996, by the American Society of Limnology and Oceanography, Inc.
An appraisal of the Allen paradox in a New Zealand trout stream
Alexander D. Huryn
Department of Zoology, POB 56, University of Otago, Dunedin, New Zealand
Abstract
Studies of invertebrate production in trout streams have often shown prey production to be insufficient
to support trout production while simultaneously providing a reasonable surplus of prey (Allen paradox).
The Allen paradox was explained by analyzing a comprehensive production budget for a trout stream in
New Zealand. Budget compartments included primary production, production by brown trout and surficial
and hyporheic macroinvertebrates, input of terrestrial invertebrates, and cannibalism by trout. Ecological
efficiencies from the literature were used to estimate food demands. Although much of the food demand by
trout was apparently derived from surficial macroinvertebrates, a balanced-budget was obtained only when
all other prey sources were included. The budget indicated that surplus production by benthic macroinvertebrates was nil. However, given the uncertainty of budget statistics, surpluses as high as - lo-20% would
probably not be detected. Secondary production by primary consumers required only -20% of total primary
production, indicating strong top-down control of herbivory by trout. Results from this study, other recent
studies showing strong effects of trout on stream food webs, and the long tradition of the Allen paradox
suggest that in productive streams (> 100 kg wet mass trout ha-l yr- I) trout may consume most (> 80%)
benthic prey production.
For the past four decades, analyses of production budgets for trout streams have generally shown that prey
reliable estimates. Most estimates of total available prey
production is insufficient to support trout production while
simultaneously
providing a reasonable surplus of prey
1988), so it is usually concluded the Allen paradox exists
because important food resources used by trout are underestimated. Although they are recognized as important
are thought
(Waters 1988). This discrepancy, first described by Allen
(195 l), is known as the Allen paradox (Hynes 1970).
Waters (1988) reviewed the historical and current status
of the Allen paradox and concluded that of 12 trout streams
for which
information
on production
by the macroin-
vertebrate community was provided, data from only two
streams showed a reasonable surplus of prey production
(Bere Stream, England; Hinau Stream, New Zealand). The
remaining studies provided estimates of prey production
that were too low to support observed trout production.
Although recognition of the Allen paradox as an important methodological challenge has continued to the present day (Benke 1993; Allan 1995), there have been few
comprehensive attempts to provide balanced production
budgets for trout streams (Waters 1988, 1993).
The Allen paradox is problematical because it suggests
that methods currently used to construct production budgets lack the precision or accuracy needed to provide
Acknowledgments
I acknowledge the assistance of C. J. Arbuckle, V. M. Butz
Huryn, and R. G. Young. Additional assistance in the field and
laboratory was provided by A. S. Flecker, E. D. Edwards, B.
Hollow, L. Kirk, F. J. Lester, K. Suberkropp, R. T. Wass, and
N. Whitmore. M. R. Scarsbrook first showed that Olinga occurs
deep within the hyporhcos. M. McDonald granted accessto the
field site. T. J. Kwak supplied the software used to estimate trout
production and biomass. Important logistical support was provided by V. Allen and M. McKenzie. Comments from S. Twombly enhanced the clarity of an earlier version of the paper.
This research was supported by grants from the New Zealand
Foundation for Research Science and Technology and the Division of Sciences, University of Otago.
to be biased toward
the low side (Waters
qualitative components of salmonid food webs, prey from
riparian sources, the hyporheic zone, or from cannibalism
are almost never quantified (Waters 1988, 1993). Uncertainty about the Allen paradox is further compounded by
lack of knowledge concerning the ecotrophic coefficient the proportion of prey production removed by harvest or
consumption (Ricker 1946). Regardless of the detail included in any budget, the ability to ascertain whether a
budget is balanced is severely compromised by difficulties
in estimating the precision of production estimates (Morin et al. 1987).
In this paper, the Allen paradox is explored by analyzing a comprehensive production budget for a high-country trout stream in New Zealand. Data comprising the
different compartments of the budget were collected from
November
199 1 through
December
1994. Major
com-
partments include annual production by primary producers, primary and secondary consumers (surficial and
hyporheic macroinvertebrates), and brown trout (Salmo
trutta L.). Additional compartments include annual input
of terrestrial invertebrates and potential cannibalism by
trout. Ecological efficiencies from the literature were used
to estimate food demands for each category of consumers.
Finally, estimates of uncertainty are provided for each
compartment.
Study site
Sutton Stream is a tributary of the Taieri River in the
southeastern part of South Island, New Zealand (Fig. 1).
The Sutton Stream catchment, which lies between the
Lammerlaw and the Rock and Pillar ranges, is incised
243
244
Huryn
Taieri
River
Catchment
Fig. 1. Map of New Zealand showing location of the Taieri
River catchment and Sutton Stream.
and rugged, with bedrock composed entirely of schist. At
the study site, the altitude is -600 m and the aspect is
NE. Land cover is mainly introduced pasture grassesand
native tussock grasses. Land use consists of extensive
grazing by livestock. The 400-m study reach has no canopy, although there are native shrubs (e.g. Coprosma spp.,
Carmichaelia sp.) along the stream margins. The channel
form is debris regulated and composed mainly of runs
and cascades with substrata consisting of poorly sorted
rubble. The stream has an average width of 3.6kO.2 m
(x+ SE). During the study, mean discharge was 175 + 62
liter s-l, and concentrations of P04- and N03- were 8 * 1
and 30 & 2 1 pg liter- l. Average daily water temperature
ranged from 0.0 to 19.5”C with an annual average of
6.2”C; diel fluctuation may be as high as 10°C during
summer. Sutton Stream is inhabited by an abundant population of brown trout probably introduced to the lower
reaches before 1890 (Thompson 1922). The trout are not
harvested by anglers. There are no other fish species in
the study reach. Further information about Sutton Stream
is available elsewhere (Young et al. 1994).
Methods
Primary production - Primary production was estimated by measuring 14C uptake by substrata placed in
submersed 17-liter recirculating chambers. Samples, sized
to -9 cm2 with a mallet and chisel, were taken from 12
randomly selected locations on eight seasonal dates between December 1992 and December 1993. Incubation
began at - 1300 hours with injection of 7 ml of NaH14C03
(185 MBq ml- l) into each of three chambers (four samples per chamber). After -2 h, samples were removed,
rinsed with acidified stream water, and placed in 50 ml
of dimethyl sulfoxide to extract 14C-labeled photosynthate (Filbin and Hough 1984). After extraction, two 1-ml
subsamples were taken from each extract, added to 10
ml of PCS in :!O-ml scintillation vials, and assayed with
a Packard Tri-carb 1900CA liquid scintillation analyzer.
In February 1993, the procedure was repeated with chambers completely covered with aluminum foil to estimate
uptake of 14C in complete darkness. The ratio of total
available inorganic C to available 14Cwas used to convert
dpm cm-2 h-l to mg C fixed cmm2h-l (Wetzel and Likens
1979). During each incubation, concentration of ambient
14C was monitored according to Iverson et al. (1976).
Sample areas were estimated by covering appropriate surfaces with aluminum foil and determining foil area from
its density. An:lual production (mg C m-2) was estimated
as the product of the average production between sampling intervals. the number of hours of available daylight
(excluding twilight), and a correction of - 10% for nighttime respiratic’n.
Benthic macroinvertebrates - Sixteen benthic samples
were taken or. 11 dates between December 199 1 and
December 1992 with a 900-cm2 Surber sampler fitted
with a 230-pm net. Sample locations were randomly assigned via a grid system. In areas of unconsolidated substrata, the streambed was sampled to a depth of - 10 cm.
Over bedrock substrata, a roll of terry cloth was attached
to the Surber frame, effectively sealing the sampler against
the stream botr.om. Macroinvertebrates collected by these
procedures are considered surficial. All samples were preserved in 6-8% Formalin and stained with phloxine B.
Animals were removed from the samples by hand under
15 x magnification, identified to the lowest practical taxonomic level (usually genus), and their lengths measured
(+0.5 mm).
Annual production was calculated by the size-frequency method (Benke 1984, 1993). Abundances were corrected for unequal sampling intervals according to Krueger and Martin (1980). Production was corrected for the
cohort produclion interval (CPI) following Benke (1984).
CPIs for most taxa were determined from length-frequency histograms constructed for each sarnple date. DeZeatidium (Ephemeroptera: Leptophlebiidae), Olinga
(Trichoptera: Conoesucidae), and Potamopyrgus (Prosobranchia: Hydrobiidae) were expected to be characterized by numerous overlapping cohorts (e.g. Collier and
Winterbourn 1990; pers. obs.). For these taxa, CPIs were
modeled with temperature, density, and size-specific
growth data derived from in situ rearings of individuals
in growth chambers according to Huryn (1990). The CPI
for oligochaetcs was assumed to range from 365 to 730
d (Brinkhurst and Cook 1979). Ash-free dry mass (AFDM)
was estimated from significant (P < 0.05) regressions of
In-transformed AFDM on In-transformed body length.
AFDM was determined according to Huryn (1990). Regressions were based on - 30 individuals representing the
observed size range for each of the major taxa.
The efficiency of Surber sampling was assessedby sampling replicated enclosures. Enclosures were 2-m lengths
of 36-cm-i.d. :PVC pipe cut lengthwise and anchored in
The Allen paradox
riffles. Each enclosure was filled with a heterogeneous
assortment of gravel-cobble-size particles and allowed to
colonize for - 1 month. After colonization, a drift net was
attached to the downstream end of each enclosure and
three Surber samples were taken following procedures
described above. After sampling, remaining substrata were
removed from each enclosure and elutriated. The sum of
macroinvertebrate biomass from each of the three Surber
samples, drift net, and excess substrata was assumed to
represent the true biomass in each of the three enclosures
(= B,,,). Macroinvertebrates from the Surber samples (=
&) were used to estimate B,,,. Btrueand Best.were compared with unpaired two-tail t-tests and In-transformed
data [ln(x + l)].
Hyporheic macroinvertebrates - From December 1993
through December 1994, substrata were sampled to 40
cm at eight locations with colonization pots. Pots consisted of 45-cm lengths of 10.5-cm-i.d. PVC pipe with
three 15-cm inserts. Each assembly was drilled with 1-cm
holes spaced - 1 cm apart to allow horizontal entry by
macroinvertebrates. Each insert had a 230-pm-mesh bottom to stop macroinvertebrates from traveling vertically
between inserts. Inserts were filled with graded pebbles
(16-32 mm), and the assembly was buried to a depth of
-40 cm and allowed to colonize for 3 + months. Sampling (four dates) involved removal of the pots, elutriation
of macroinvertebrates from each insert, and reburial.
Macroinvertebrates were processed as above. Macroinvertebrates > 10 cm below the streambed were considered
hyporheic.
Proportions of macroinvertebrate biomass and abundance in hyporheic inserts (e.g. lo-25- and 25-40-cm
depths) were calculated relative to the biomass and abundance within the top insert (surficial, < 10 cm). These
data were used to estimate taxon-specific biomass and
production within the hyporheos as the product of the
proportional representation of biomass in each insert and
the biomass and P : B ratios estimated from the December
199 1 through December 1992 data for surficial macroinvertebrates. This procedure was followed to account for
differences in the macroinvertebrate community between
years (1992 vs. 1994) and for differences in abundance
because of the heterogeneity of ambient substrata and the
uniform substrata used in the colonization pots. The extent of the hyporheic zone was estimated by driving a
steel rod ( 1.5-cm diam) into the streambed and measuring
the depth of penetration. Sample positions were located
at 1-m intervals along successive 30-m transects throughout the length of the study reach. From these data, I
estimated the area of streambed extending to depths > 10
cm. These estimates were used to weight hyporheic biomass and production to provide values per square meter
of streambed.
Terrestrial macroinvertebrates- Annual input of winged
insects from terrestrial sources was estimated by means
of an empirical model derived for Sutton Stream (Edwards and Huryn 1995). In summary, three 10-m sections
of the study reach were blocked with l-mm-mesh drift
245
nets. The upper net intercepted material originating above
the study section. The lower net collected material that
entered the study section. Trout were excluded from surface feeding by placing a mesh barrier over the entire
bottom of the stream between drift nets. Estimates of
biomass input, based on winged insects collected in six
24-h periods over a 1-yr period, were used to produce
the following regression model:
Bf = 0.008 T2.430;n = 6, r2 = 0.98, P < 0.001.
&is the biomass of winged insects (mg AFDM m-2 d-l)
and T is average daily water temperature (“C) (Edwards
and Huryn 1995). Annual input of winged insects was
estimated as a function of mean daily water temperature
measured from December 199 l-December 1992 with a
submersible temperature recorder. Daily inputs of wingless invertebrates of terrestrial origin did not follow predictable seasonal trends; therefore, average daily input
(l.lkO.6 mg AFDM m-2 d-l, x&SE) was used to estimate annual input (Edwards and Huryn 1995). Inputs
were assumed to be nil on days when mean temperature
was 15°C.
Trout -Trout were sampled by electric fishing on two
dates during November 199 1 and November 1992. Befort sampling, the study reach was divided into 12 subsections (-30 m) with stop nets. On the first date of each
November sampling period, trout captured during a single pass were anaesthetized, measured for length (mm)
and wet weight (0.1 g), and marked by either removing
the adipose fin or by subcutaneously injecting an aqueous
solution of Alcian Blue (Kelly 1967). Trout were resampled -2 weeks later, and abundance and biomass estimates were made with the mark-recapture module provided by Pop/Pro (Kwak 1992). On each date, ages of
trout were determined by using sectioned otoliths (Hall
1991). Estimates of age were validated by observing
marked fish and by changes in annual length-frequency
plots over a 3-yr period of additional study (1992-l 995).
During each sampling period, a subsample of trout representing the available size range was dried to constant
mass at 60°C and ashed at 500°C for a minimum of 4 h
to yield AFDM as the difference between dry mass and
ash mass. Length-specific biomass was estimated with
regressions of AFDM against length. The taxonomic composition and biomass of invertebrates comprising the
stomach contents were also determined. Trout abundance, biomass, and annual production (mg AFDM m-2’
+ 95% C.I.) were estimated with the instantaneous growth
module provided by Pop/Pro (Kwak 1992). Trout production potentially lost to cannibalism was estimated by
subtracting the biomass of the 0+ cohort remaining during the November 1992 sampling period from the production of this cohort from November 1991-November
1992.
Budget -Food demand by consumers was estimated as
the product of the reciprocal of gross production efficiency
and production, where the gross production efficiency is
the product of assimilation efficiency and net production
246
Huryn
Table 1. Summary of ecological efficiencies used to calculate food demands by different consumer groups. AE-Assimilation
efficiency (assimilation : consumption); NPE-net production efficiency (production : assimilation); GPE-gross production efficiency (production : consumption). T-Trichoptera;
D-Diptera; E-Ephemeroptem; M-Megaloptera; PL-Plecoptera.
AE
Consumers
Food
NPE
GPE
Source
(%)
Primary
Glossosoma (T)
Simulium (D)
Hydropsyche (T)
Stenonema (E)
Tricorythodes (E)
Primary/secondary
Hydropsyche (T)
Diplectrona (T)
Secondary
Corydalus (M)
Acroneuria (PL)
Acroneuria (PL)
Trout
Epilithon
Diatoms
Diatoms
Diatoms
Diatoms
24
57
36-49
53
28-47
26
51
70
27
65
6
29
25-34
14
18
Algae/ Tubifex
Algae/Tubifex
-
41-52
44-5 1
-
Edington and Hildrew 1973
Edington and Hildrew 1973
Chironomids
Chironomids
82
80-86
86
66
41
56
33
Brown and Fitzpatrick 1978
Brocksen et al. 1968
Heiman and Knight 1975
Four studies summarized by
Waters 1988
Calculated for Sutton Stream
following Elliot 1976
Hydropsyche/Simulium
Salmo trutta
Invertebrates
-
-
16-23
S. trutta
Amphipods
-
-
23
Because I did not measure ecological efficiencies, I calculated food demand by means of efficiencies
Cummins 1975
McCullough et al. 1979a
McCullough et al. 1979a
Trama 1972
McCullough et al. 19793
Estimates
of uncertainty-Approximate
9 5% confidence intervals were derived for budget statistics by bootstrapping-a nonparametric resampling technique (Effron and Tibshirani 1993). Bootstrapping is used to estimate the uncertainty of variables with unknown or complex frequency distributions and for situations in which
consumer food demand). For each vector, a mean and
approximate 95% C.I. (C.I.,) was calculated by the biascorrected percentile method (Meyer et al. 1986).
For specific parameters, the bootstrapping procedure
was modified. First, for estimates of macroinvertebrate
production using the size-frequency method, choice of
CPI has large oonsequences for final values (Short et al.
1987), but the error associated with this parameter has
never been included in calculations of the uncertainty of
size-frequency production estimates (Krueger and Martin
1980; Morin et al. 1987; Short et al. 1987). In practice,
CPI is usually derived as the median period required for
the completion of somatic growth by the individuals comprising a cohort. To account for the uncertainty inherent
in this procedure, I assumed that estimates of CPI are
normally distr: buted about the median with 95% confidence boundaries that include the minimum and maximum possible CPI as determined from field data. A normal distribution constructed on the basis of these parameters was used to produce a vector of 1,000 randomly
logistical
drawn values. These values were used to adjust the vector
efficiency.
summarized from the literature following the method of
Benke and Wallace (1980). Although any single estimate
should be suspect, groups of efficiencies selected from
diverse sources are generally consistent for a given category of consumers (Pandian and Marian 1986). The
sources and values of ecological efficiencies are summarized in Table 1. Food demand was estimated for each
trophic category: macroinvertebrate browsers of stone organic layers (primary consumers), predatory macroinvertebrates (secondary consumers), and brown trout (top
consumer).
constraints
do not allow sufficient
replication
(e.g. production studies, Morin et al. 1987). At minimum,
bootstrapping provides an estimate of the uncertainty
inherent in a particular data set and the methods used to
describe a given parameter. However, if the data are unbiased and of sufficient coverage, bootstrapping will provide an estimate of the true probability distribution underlying that parameter (Effron and Tibshirani 1993). Estimates of uncertainty for this study were derived by randomly resampling every data set with replacement until
1,000 data sets were produced. These recombined data
sets were used to produce vectors of 1,000 estimates for
each parameter (production, biomass, P : B, abundance,
of bootstrap estimates of uncorrected production. Second,
vectors of trout production were compiled with values
randomly drawn from a normal distribution constructed
on the basis of descriptive statistics provided by the original estimate (Kwak 1992).
Results
Primary
proakction
-Temporal
variation
of primary
production was strongly seasonal, ranging from 11+ 3 mg
C mm2h-l (x? SE) in July (austral winter) to 113 + 22 in
,
247
The Allen paradox
Primary
production
Primary
consumer
demand
Primary
consumer
productlon
Primary
consumer
production
Secondary
consumer
demand
Secondary
consumer
production
Benthic
secondary
productlon
Trcut
production
Trout
demand
Fig. 2. Estimates of primary production and consumer production and demand for Sutton
Stream. (Note change in scale.) Error bars = 95% bootstrap confidence intervals.
February (austral summer). Substrata incubated in total
darkness showed rates of 14C uptake -3% of those incubated under ambient afternoon light. Annual primary
production was estimated to be 155 + 37 g C m-2 (x+ 95%
C.I+). Because periphyton in Sutton Stream is predominantly composed of diatoms (pers. obs.), carbon values
were converted to AFDM using a factor of 2 x (=3 10 + 74
g AFDM m-2 yr- l; Fig. 2) (McCullough et al. 1979a).
Eficiency of surjcial sampling- Mean biomass was underestimated for nine and overestimated for 10 taxa; however, a significant differences (P < 0.05) between Best.and
B,,, were detected only for Psilochorema and Tiphobiosis
(Table 2). Taxa that were major contributors to secondary
production had P-values ranging from 0.20 to 0.96 (Table
2).
Surficial primary consumers-Total surficial production
by primary consumers was 11,209 f 2,294 mg AFDM m-2
yr-l (x+C.I.,), and P: B was 6.9+ 1.3. The major contributor was the diamesine chironomid Maoridiamesa
(Table 3). This substantial production (25% of total) was
due to relatively high biomass and a bivoltine life cycle.
Other chironomids, primarily the Orthocladiinae (morphotype “a,” cf. Cricotopus, Eukiefiriella; Table 3), contributcd an additional 10% to total surficial production.
The relatively high collective P : B of the chironomids (10.7)
greatly influenced the grand P: B, which was reduced to
5.8 when chironomids were excluded. Becauseof relatively
short CPIs and high turnover rates (P: B = 9-l 7), Deleatidium (17%), Austrosimulium (1O%), and Zelandoperla
(8%) also showed substantial production. Other major contributors, Olinga (9%) and Aoteapsyche (7%), had moderate P: B (3-7) but relatively high biomass. Because it is
an omnivore (Crosby 1975; Hopkins 1976), production
by Aoteapsyche (1,855 mg AFDM m-2 yr-l) was divided
between primary (40%) and secondary consumers (60%)
following Hopkins (1976) and Benke and Wallace (1980).
Hyporheic primary consumers-Measurements taken at
406 locations showed that 49% of the streambed extends
to depths 5 10 cm (includes exposed bedrock, 27%), 37%
extends from lo-25 cm, and 11% extends from 25-40 cm.
Only 3% of the streambcd extends to depths >40 cm. The
hyporheic zone of Sutton Stream is limited in extent because the channel is highly constrained by bedrock.
Total production by hyporheic primary consumers was
2,144+ 1,500 mg AFDM mm2 yr-l (x&C.I.,), and P : B
was 4.4 (Table 4). Major contributors included Olinga
(40%), Oligochaeta (19%), and Potamopyrgus (15%). The
chironomids contributed substantially less to hyporheic
compared to surficial production (17 vs. 35%). Only the
Oligochaeta showed higher hyporheic than surficial production, although the difference is not significant (cf. C.I+,
Tables 3, 4).
Table 2. Summary statistics for assessment of efficiency of
surficial sampling. II,.,. - Composite mean of three Surber samples taken from each of three colonized enclosures; B,,, - mean
of total macroinvertebrate biomass in each of three colonized
enclosures; P-result of two-tail unpaired t-test comparing II,,,,
and B,,, (df = 4) with ln(x + 1) - transformed data. TTrichoptera; D- Diptera; M - Megaloptera; E- Ephemeroptera; G-prosobranch gastropod; PL-Plecoptera.
B est.
Aoteapsyche (T)
Aphrophila (D)
Archechauliodes (M)
Austrosimulium
(D)
Coloburiscus (E)
Deleatidium (E)
Hydrobiosis (T)
Maoridiamesa
(D)
Neurochorema (T)
Oligochaeta
Olinga (T)
Orthocladiinae (D)
Polyplectropus (T)
Potamopyrgus (G)
Psilochorema (T)
Pycnocentria (T)
Stenoperla (PL)
Tiphobiosis (T)
Zelandoperla (PL)
B true
(mg AFDM
263
1
143
38
432
413
48
79
10
1
332
29
<l
<l
5
3
48
4
53
m-2) Btrue : B,,,.
304
1.16
1
0.81
278
1.95
23
0.59
719
1.66
484
1.17
63
1.30
43
0.54
3
0.35
<l
0.23
475
1.43
13
0.46 ’
<l
0.00
1
2.78
10
0.74
3
1.80
57
1.18
3
0.64
57
1.07
P
0.69
0.91
0.20
0.96
0.42
0.68
0.48
0.35
0.92
0.15
0.72
0.12
0.37
0.43
0.02
0.71
0.25
0.03
0.50
248
Huryn
Table 3. Summary of production data for primary consumers from substrata < 10 cm below bed of Sutton Stream. N-Abundance
(ind. m-“); B-bi omass (AFDM, mg m-‘); P-production (AFDM, mg rnb2 yr - l). N, B, P given + 95% C.I. CPI,i, and CPI,,, Apparent minimum (maximum) cohort production intervals (d). 0+ and 2 + yr pi.ey-Biomass of macroinvertebrate taxa taken
from 0 + yr (n = 13) and 2+ yr (n = 33) trout collected in November 199 1 and November 1992; prey biomass (mg AFDM) given
per unit trout biomass (g AFDM) + SE. D-Diptera;
E-Ephemeroptera; T-Trichoptera;
PL-Plecoptera; G-prosobranch
gastropod; C-Coleoptera. Taxa arranged in order of decreasing production.
Maoridiamesa
(D)*
Maoridiamesa
(D)?
Deleatidium (E)
Olinga (T)
Austrosimulium
(D)*
Austrosimulium
(D)Jf
Zelandoperla (PL)
Helicopsyche (T)
Aoteapsyche (T)$
Orthocladiinae “a” (D)*
Orthocladiinae “a” (D)“f
Potamopyrgus (G)
Aphrophila (D)
Oligochaeta
Tanytarsini (D)*
Tanytarsini (D)t
cf. Cricotopus (D)*
cf. Cricotopus (D)t
Coloburiscus (E)
Eukiefiriella
(D)
Miscellaneous$
Chironomini (D)
Hydora (C)
Austroclima (E)
Pycnocentria (T)
Pycnocentrodes (T)
N
B
P
440(169)
947(36 1)
1,197(310)
782(192)
187(153)
377(90)
343( 147)
658(132)
198(89)
1,242(329)
1,095(214)
1,528(38 1)
422(90)
2,950( 1,320)
141(39)
88(33)
117(45)
259( 100)
364( 142)
236(60)
78 1(396)
11l(66)
38(18)
39(24)
50(36)
81(24)
180(67)
25(16)
7(4)
6(5)
3(3)
6(4)
15,199(1,770)
85(32)
197(68)
109(27)
3 18(63)
12(10)
55(19)
105(46)
135(27)
106(56)
W6)
1w
182(43)
77(16)
W8)
5(2)
w
4(2)
8(3)
54(24)
W)
22( 11)
14(7)
14(7)
7(3)
14(8)
5(2)
4(2)
5(4)
3(2)
l(1)
l(l)
O(1)
1,629(146)
1,035(770)
1,776(845)
1,855(1,514)
1,002(2 15)
504(42 1)
578(1,145)
943(88 1)
833(378)
742(490)
342(207)
240(45 1)
537(250)
418(171)
316(175)
141(68)
23(19)
67(44)
79(30)
134(59)
131(39)
1lO(-)
69(48)
45(28)
43(25)
39(37)
28(19)
23(12)
23(23)
1W)
1O(8)
2(l)
l(l)
11,209(2,294)
Orthocladiinae (D)
Zeolessica (T)
Nesamaletus (E)
Hydrobiosella (T)
Austroperla (PL)
Ptilodactylidae (C)
Total
* Summer/fall cohort.
t Fall/summer cohort.
$ Suspected omnivore, N, B, P weighted by 40% (see text).
0 Primarily meiofauna, P estimated as B x 5.
Secondary consumers - Total production by surficial
secondary consumers was 2,144 + 774 mg AFDM mm2yr- 1
(xfC.I+), and P: B was 4.1 kO.9 (Table 5). Major contributors were Aoteapsyche (5 2%) and Archechauliodes
(33%). Recall that production by Aoteapsyche was divided
between primary consumers (40%) and secondary consumers (60%). The relatively high P : B of Aoteapsyche (7) had
a substantial effect on overall P: B, which is reduced to
2.8 when Aoteapsyche is excluded. This relatively low P :
B is due to long CPIs.
Total production by hyporheic secondary consumers was
392+274 mg AFDM m-2 yr-l (xkC.I.J, and P:B was
3.1 (Table 6). Major contributors were Archechauliodes
(49%), Aoteapsyche (24%), and the Tanypodinae (16%).
CPI,,
74
113
107
‘538
51
61
90
214
,214
66
66
365
166
365
32
66
66
182
579
76
182
365
1!75
243
:!43
:.82
I!43
Z!59
76
:‘32
300
CPI,,,
0+ yr prey
2+ yr prey
174
0.48(0.19)
214
273
1.47(0.57)
758
0.24(0.24)
71
0.02(0.02)
273
1.21(0.73)
289
424
0.01(0.01)
427
1.02(0.65)
-154
182
730
334
O.&l
2)
-730
-66
182
154
0.01(0.01)
211
730
0.28(0.28)
-182
--365
-730
-441
609
609
o.o7(;05)
-365
-609
-471
-151
-822
-400
P:B = 6.88 (1.27)
0.35(0.19)
0.48(0.19)
3.21(1.07)
0.0 l(O.00)
0.45(0.19)
0.57(0.10)
0.85(0.23)
~0.01(<0.01)
0.23(0.08)
0.13(0.07)
-~0.01(<0.01)
0.98(0.3 1)
~0.01(<0.01)
---0.1;(0;7)
0.30(0.08)
-------
Only the Tanypodinae and Amelotopsis showed higher hyporheic than surficial production, although the difference
is not significant (cf. C.I+, Tables 5 and 6).
Terrestrial macroinvertebrates - The predictive relationships derived for Sutton Stream by Edwards and Huryn
(1995) indicated that inputs of wingless and winged terrestrial invertebrates in December 199 l-December 1992
were208f203and423k108mgAFDMm-2yr-1(x495%
C.I.& Total annual input was estimated to be 63 1k 230
mg AFDM m-2 yr-l.
Trout -The population of brown trout in the study reach
is stunted (e.g. Hall 1991) and nonmigratory. Individuals
249
The Allen paradox
Table 6. Summary of production data for secondary consumers from substrata > 1O-40 cm below bed of Sutton Stream.
Abbreviations and units as in Table 3. Taxa arranged as in Table
5 to aid in comparison with surficial production.
Table 4. Summary of production data for secondary consumers from substrata > 1O-40 cm below bed of Sutton Stream.
Abbreviations and units as in Table 3. Taxa arranged as in Table
3 to aid in comparison with surficial production.
Maoridiamesa
(D)
Deleatidium (E)
Olinga (T)
Austrosimulium
(D)
Zelandoperla (PL)
Helicopsyche (T)
Aoteapsyche (T)*
Orthocladiinae “a”
0
N
B
177(522)
143(72)
284( 142)
28(33)
-
13(109)
7(2)
269( 122)
400)
-
127(1,117)
64(54)
846(393)
60(2 15)
-
1960)
9(15)
62(120)
N
P
191(128)
957(683)
65(230)
1,910(1,450)
64(108)
3 1(22)
41(91)
19(14)
31(31)
29(30)
21(12)
Tanypodinae (D)
78;;)
fm
<I
-
13(24)
78(74)
l(7)
20(19)
<W)
-
93(180)
192(192)
4(18)
63(56)
4(6)
-
2863)
977)
Polyplectropus (T)
< l(21)
3(15)
<l(4)
Total
176(109)
125(8 1)
392(274)
* Suspected omnivore, N, B, P weighted by 60% (cf. Hopkins
1976; Benke and Wallace 1980).
67(80)
5(4)
109(78)
3 19(308)
l(129)
5(700)
Oligochaeta
402(507)
43(44)
Tanytarsini (D)
106(129)
5(4)
cf. Cricotopus (D)
17(17)
2(l)
Coloburiscus (E)
24(28)
lO(10)
Eukiefiriella
(D)
< l(l)
1w3)
Chironomini (D)
22(25)
4(5)
Hydora (C)
Austroclima (E)
< l(l)
3;)
36)
Pycnocentria (T)
2(4)
l(l)
l(6)
Pycnocentrodes (T)
Orthocladiinae (D)
15(11)
3G)
<l(l)
Zeolessica (T)
Nesamaletus (E)
Hydrobiosella (T)
Austroperla (PL)
Ptilodactylidae (C)
Total
3,853(1,806) 483(222) 2,144(1,501)
* Suspected omnivore, N, B, P weighted by 40% (cf. Hopkins
1976; Benke and Wallace 1980).
Potamopyrgus (G)
Aphrophila (D)
Aoteapsyche (T)*
Archechauliodes (M)
Hydrobiosis (T)
Psilochorema (T)
Stenoperla (PL)
Neurochorema (T)
Tiphobiosis (T)
Amelotopsis (E)
P
B
31(16)
Empididae (D)
have been encountered and no marked fish have been
recovered from locations outside the 400-m study reach.
From November 199 1 through November 1992, productionbytroutwas2,069+114mgAFDMm-2yr-1(x+SE)
or 114 kg WM ha-l using the AFDM to wet mass (WM)
conversion given by Waters (1988). The P : B was 1.O+ 0.1.
Although the population is stunted, relatively high production was attained because of high abundances (0.7 &O. 1
trout m-2).
Production by 0+ yr trout (i.e. spawned in autumn 199 1)
was 542+32 mg AFDM m-2 yr-l (x&SE, 26% of total
production) and P : B was 3.9. The difference between the
November 1992 biomass (281+34 mg AFDM m-2) and
the November 199 l-November 1992 production by 0+
yr trout provides a liberal estimate of trout available for
cannibalism: 262 & 126 mg AFDM m-2 yr- l (x&95% C.I.,).
The potential for cannibalism is trivial compared to other
prey sources (Fig. 3).
achieve lengths of only - 170 mm by the third year of
growth. The oldest fish encountered during the study (- 56 yr) generally had lengths ~220 mm. During 3 yr of
additional study (1992-1995, unpubl.) no fish >250 mm
Table 5. Summary of production data for secondary consumers from substrata < 10 cm below bed of Sutton Stream. Abbreviations and units as in Table 3. Taxa arranged in order of decreasing production.
Aoteapsyche (T)*
Archechauliodes (M)
Hydrobiosis (T)
N
B
P
296(135)
86(2 1)
97(22)
99(46)
50(15)
5(2)
1w5)
24(14)
3(2)
22( 11)
5(3)
409(59)
158(87)
28 l(57)
W7)
19(14)
7(2)
22(15)
12(5)
w
4(3)
W)
l(l)
532( 105)
1,113(736)
698(204)
73(22)
60(38)
55(33)
54(3 1)
53(20)
cplmin
214
668
608
244
138
641
306
214
365
181
244
cmlax
427
1,034
806
393
320
701
396
377
730
393
455
P : B = 4.12 (0.93)
Tanypodinae (D)
Psilochorema (T)
Stenoperla (PL)
Neurochorema (T)
Tiphobiosis (T)
15(5)
Amelotopsis (E)
12(9)
Empididae (D)
9(7)
Polyplectropus (T)
3(3)
2,144(774)
Total
* Suspected omnivore, N, B, P weighted by 60% (cf. Hopkins 1976; Benke and Wallace 1980).
0+ yr prey
1.02(0.65)
1.07(0.93)
--
2+ yr prey
0.1;(0;7)
---
0.02(0.0 1)
0.17(0.12)
0.03(0.02)
0.2<(0;5)
O.Ol(O<l)
-
o.os(o;5,
0.85(0.23)
0.92(0.56)
0.26(0.11)
I
1
250
Huryn
16000
12000
‘;
Cu%
‘E
I
1
IT T
8000
:
E
4000
Fig. 3. Comparison of total prey available for consumption
by trout and breakdown of prey from different sources. Error bars
= 95% bootstrap confidence intervals.
Stomach contents were analyzed for 13 0+ and 33 2+
yr trout collected in November 199 1 and November 1992.
Deleatidium (22%), Zelandoperla ( 18%), Archechauliodes
(16%) and Aoteapsyche (15%) comprised most of the late
spring diet of 0+ yr trout. Olinga (34%), Coloburiscus
(lo%), Archechauliodes (lo%), and Aoteapsyche (9%) were
major contributors to the late spring diet of 2+ yr trout.
Relative amounts of the different prey taxa roughly reflected relative levels of production (Tables 3 and 5). Tcrrestrial invertebrates were important components of late
spring diets, contributing 2.4 +_2.2 (20%) and 3.7 +,2.0 (28%)
mg AFDM prey g AFDM trout- l (x+ SE) for 0 + and 2 +
yr trout.
Budget -Mean values of assimilation and net production efficiencies used to estimate food demand by primary
consumers were 42 & 9 and 46 + 10% (x-+ 95% C.I+; Table
1). The estimates of food demand by primary consumers
(surficial + hyporheic) based on these efficiencies was
66228 g AFDM mm2 yr- l (Fig. 2). Note that the bootstrapping procedure results in bias-corrected means that
vary slightly from calculations based on absolute means.
Surplus primary production was 244*79 g AFDM m-2
yr-’ (-79% of total). The 95% CT+ values do not overlap,
showing that surplus primary production is significantly
higher than consumer demands. Mean values of assimilation and net production efficiencies used to estimate food
demand by secondary consumers were 85 + 3 and 52 + 9%
(x*95% C.I+; Table 1). The estimates of food demand by
secondary consumers (surficial + hyporheic) was
5,538+2,486 mg AFDM m-2 yr-l (Fig. 2). Surplus production by primary consumers was 7,8 16+ 3,484 mg
AFDM rnM2yr-l.
The mean value for the gross production efficiency used
to estimate food demand by trout was 18f 4% (X f 95%
CL,; Table 1). Because the population of trout is stunted,
the true gross production efficiency might be lower than
published values, which would result in higher actual food
demands (Elliot 1994). Food demand by trout was
11,282+2,885 mg AFDM m-2 yr-l (x+95% C.I+,, Figs.
2, 3), assuming a gross production efficiency of 18%. If the
trout population of Sutton Stream consumed only benthic
macroinvertebrates (surplus primary consumer + secondary consumer production), an apparent deficit of benthic
secondary production would occur (- 930&4,370 mg
AFDM m-2 yr - l; Fig. 2). If the trout population consumed
all available l;errestrial invertebrate biomass (63 1 mg
AFDM m-2 yr-‘) and all 0+ fish available for cannibalism
(262 mg AFDM m-2 yr- ‘) with benthic invertebrates composing the balance of their food demand, a slight deficit
would still be apparent (-37f4,367 mg AFDM m-2 yr-l;
Fig. 3). Note that for both estimates, 95% C.I+, values show
that surplus benthic secondary production is not significantly differen from zero.
Discussion
Maximum d sily primary production measured in Sutton
Stream is within the range expected for open streams with
moderate levels of nutrients (e.g. <2 g C m-2 d-l; Allan
1995). Annual primary production was within the maximum range expected for freshwater systems worldwide
(e.g. ~200 g C m-2 d-l; Bott 1983). Although primary
production was measured in 1992 and consumer production was measured in 199 1, the relationship between trophic levels probably was consistent between years. Trout
.production in 199 1 (2,069 mg AFDM m-2) was similar
to production in 1992 (2,187 mg AFDM m-2, unpubl.)
and, assuming that the ecotrophic coefficient was similar
between years, primary consumer production and demand
probably were illso similar. Therefore, if primary consumers feed only on autotrophs, a substantial and significant
surplus of primary production (-79%) is predicted. Because a portion of primary consumer production is undoubtedly deri ved from autochthonous or allochthonous
detritus (Strayer 1988), the surplus of primary production
reported here :s conservative. Coarse allochthonous detritus, primarily tillers from tussock grass, is apparently
not directly consumed by macroinvertebrates (Young et
al. 1994); however, fine particulate or dissolved organic
matter may comprise a significant allochthonous source
of food for primary consumers.
In a manner parallel to that observed for primary production and primary consumers, a substantial surplus of
primary consumer production remains after the demands
of the secondary consumers are accounted for. Much of
the food demand by secondary consumers may consist of
meiofaunal invertebrates that are systematically underestimated by traditional sampling methods (Waters 1993).
Substantive USCof meiofauna by secondary consumers
would tend to increase the amount of macroinvertebrate
production available to trout (Waters 1993). Although the
prey of secondary consumers in Sutton Stream was not
studied, this factor has been studied in detail elsewhere in
The Allen paradox
New Zealand. The prey of Aoteapsyche, Archechauliodes,
Hydrobiosis, Psilochorema, and Stenoperla is largely larval
chironomids, simuliids, and Deleatidium (Crosby 1975;
Devonport and Winterbourn 1976; Winterbourn 1978).
Although more research is needed in this area, most of the
food supporting secondary consumers is assumed to be in
the form of macroinvertebrates rather than meiofauna.
The annual production of trout in Sutton Stream (- 110
kg WM ha-l) is comparable to levels of production used
to define highly productive trout streams elsewhere (- 1OO300 kg WM ha-l; Waters 1988, 1992). The P: Bratio (1.0)
is also comparable to other trout populations with similar
age structure (Waters 1992). Current knowledge indicates
that Sutton Stream should show a deficit or a near-deficit
of benthic prey production relative to demands by trout
(the Allen paradox) (Waters 1988, 1993).
In the past, production budgets for trout streams have
been constructed on the premise that prey production is
largely equivalent to production by surficial macroinvertebrates (Waters 1.988). Following this tradition, one can
clearly see the spectre of the Allen paradox in the budget
constructed for Sutton Stream (Fig. 3). This deficit of surficial macroinvertebrate production relative to trout demands often has been attributed to sampling inefficiency
(Allen 195 1; Waters 1988); however, a test of the efficiency
of the sampling of surficial substrata in Sutton Stream
showed little significant bias (Table 2).
After one considers the relative importance of each component of the budget, it is apparent that a balanced budget
is observed only when sources of trout prey in addition to
surficial benthos are included (Fig. 3). Terrestrial invertebrates are an important food resource for trout (e.g. Hunt
1975); however, the role of hyporheic fauna as prey is not
well understood. Behavioral observations (A. R. McIntosh
pers. comm.) and case characteristics of Olinga indicate
diel burrowing behavior, as was shown for the sericostomatid caddisfly Gumaga in California streams (Bergey and
Resh 1994). Because Olinga is a major component of the
hyporheos and an important prey species for trout in Sutton Stream (Tables 3, 4), burrowing behavior may form a
link between trout production and the hyporheos. Nevertheless, prior to emergence, hyporheic insects must enter
the surficial sediments and the water column where they
are subject to trout predation.
Ecotrophic coefficients traditionally expected for trout
streams are generally in the range of 30-50% (Waters 1988).
However, published estimates of the proportion of lotic
insect production emerging as adult biomass indicate that
ecotrophic coefficients often may be considerably > 50%.
Jackson and Fisher ( 1986) reported that only 19% of the
benthic insect production of Sycamore Creek (Arizona)
emerged as adult biomass. Jackson and Fisher reviewed
similar studies of stream insect communities to show that
the proportion of annual production that emerges as adult
biomass is generally <20% (range, 4-23%). Although far
from exhaustive, these studies indicate that -80% of the
annual production of lotic insect populations commonly
may be lost to other pathways, and estimates of ecotrophic
coefficients > 80% for stream invertebrate communities
seemreasonable. Surplus benthic production expected from
251
Sutton Stream would be 5 3,000 mg AFDM m-2 following
this rationale and probably would not be detectable given
the uncertainty estimated for the budget compartments
(cf. 95% C.I+,, Figs. 2, 3).
Within the constraints of the estimated uncertainty, surplus production by primary consumers in Sutton Stream
clearly is extremely low. Consequently, it seems logical to
suspect that the expected surplus of primary production
(-79%; Fig. 2) is the result of top-down control of herbivory by trout as was shown in the nearby Shag River by
Flecker and Townsend (1994). They used abundances of
trout that were based on the Sutton Stream population and
replicated enclosures (A. S. Flecker pers. comm.), and
showed that over a period of 10 d, trout were associated
with a -2-fold reduction in macroinvertebrate biomass
and a -4-fold increase in periphyton biomass compared
with fishless treatments. The results of the production budget presented here, and perhaps the results of other budgets
that show the Allen paradox (Waters 1988), are supported
by recent experimental studies that show dramatic effects
of salmonids on prey populations in moderately to highly
productive trout streams (Bechara et al. 1992; Flecker and
Townsend 1994).
It may be time to adopt a new perspective about trout
streams and the Allen paradox. Rather than viewing the
Allen paradox as a paradox per se or as a simple methodological nightmare, it may be more constructive to accept the challenge of a messagethat has been conveyed for
decades: in productive streams (i.e. lOO+ kg WM trout
ha- l yr- l), trout can be expected to consume an extremely
large proportion of benthic prey production, perhaps > 80%.
After one considers the uncertainty terms estimated for
the compartments of the Sutton Stream budget (Figs. 2,
3), it is clear that the constraints of systematic error and
natural variability often will preclude detection of such
small surpluses.
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Submitted: 30 May 1995
Accepted: 28 August 1995
Amended: 7 November 1995