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DETERMINANTS OF GROWTH AND SURVIVAL OF LARVAL PALLID
STURGEON: A COMBINED LABORATORY AND FIELD APPROACH
BY
TOBIAS RAPP
A dissertation submitted in partial fulfillment of the requirements for the
Doctor of Philosophy
Major in Wildlife and Fisheries Sciences
South Dakota State University
2014
iii
ACKNOWLEDGEMENTS
I thank my advisor Dr. Brian Graeb and my co-advisor Dr. Steven Chipps for their advice
and guidance during my time at SDSU. I thank my committee member Dr. Robert Klumb
for his advice and support of the research projects. I also want to thank my committee
member Dr. Michael Brown for his advice when I had questions about fish aquaculture.
I thank the secretary in the Department of Natural Resource Management Dawn Van
Ballegooyen, Diane Drake, Carol Jacobsen, Terri Symens, and Kate Tvedt for making my
life easier.
I thank the hatchery personnel at Gavins Point Dam National Fish Hatchery and Garrison
Dam National Fish hatchery for providing pallid sturgeon for the research projects and
the personnel at Gavins Point Dam National Fish hatchery for providing logistic support
during field work.
The research projects would not have been possible without the help of many technicians
and graduate students, who are listed in the acknowledgements of the individual chapters.
Funding was provided by the U.S. Army Corps of Engineers (3F9172)
iv
TABLE OF CONTENTS
LIST OF FIGURES ........................................................................................................... vi
LIST OF TABLES ............................................................................................................ xii
ABSTRACT ..................................................................................................................... xvi
CHAPTER 1: INTRODUCTION ....................................................................................... 1
REFERENCES ............................................................................................................... 7
CHAPTER II: GROWTH AND SURVIVAL OF LARVAL PALLID STURGEON AT
THE ONSET OF EXOGENOUS FEEDING IN RESPONSE TO DIFFERENT PREY
TYPES .............................................................................................................................. 12
ABSTRACT .................................................................................................................. 12
INTRODUCTION ........................................................................................................ 13
METHODS ................................................................................................................... 17
RESULTS ..................................................................................................................... 21
DISCUSSION ............................................................................................................... 23
ACKNOWLEDGEMENTS .......................................................................................... 30
REFERENCES ............................................................................................................. 31
CHAPTER III: ONTOGENY OF THE FEEDING ECOLOGY IN PALLID
STURGEON: SEQUENCE OF PREY SELECTION AND FOOD HABITS FROM
FIRST FEEDING LARVAE TO AGE-2 JUVENILE FISH ............................................ 42
ABSTRACT .................................................................................................................. 42
v
INTRODUCTION ........................................................................................................ 43
METHODS ................................................................................................................... 49
RESULTS ..................................................................................................................... 56
DISCUSSION ............................................................................................................... 60
ACKNOWLEDGEMENTS .......................................................................................... 67
REFERENCES ............................................................................................................. 68
CHAPTER IV: SHALLOW WATER HABITAT EVALUATION IN THE LEWIS AND
CLARK DELTA, WITH A FOCUS ON NURSERY HABITAT SUITABILITY FOR
PALLID STURGEON ...................................................................................................... 91
ABSTRACT .................................................................................................................. 91
INTRODUCTION ........................................................................................................ 93
METHODS ................................................................................................................... 97
RESULTS ................................................................................................................... 106
DISCUSSION ............................................................................................................. 115
ACKNOWLEDGEMENTS ........................................................................................ 130
REFERENCES ........................................................................................................... 131
CHAPTER V: SUMMARY ............................................................................................ 167
REFERENCES ........................................................................................................... 172
vi
LIST OF FIGURES
Figure 2-1: Mean ± SE total length (mm; open circles) and mean ± SE yolk volume
(mm3; closed circles) of larval pallid sturgeon from day 5 to 13 post-hatch. Physiological
age, expressed as cumulative thermal units, is given in brackets. Differences between
prey types were not significant and presented data is pooled over all treatments (growth:
repeated measures ANOVA, treatment effect: F = 1.040, df = 4, P = 0.41, yolk volume:
repeated measures ANOVA, treatment effect: F = 0.130, df = 4, P = 0.97). Arrows
indicate the first ingestion of the different prey types (Z = zooplankton, C =
Chironomidae larvae, E = Ephemeroptera larvae). ........................................................... 38
Figure 2-2: Mean ± SE percentage of feeding pallid sturgeon in response to different
prey types at (A) day 12 post-hatch (Kruskal-Wallis-H, χ2 = 9.350, df = 3, P = 0.03) and
(B) day 13 post-hatch (Kruskal-Wallis-H, χ2 = 1.724, df = 3, P = 0.63). ........................ 39
Figure 2-3: Initial (closed bar) and final (open bar) mean ± SE total length (mm) of
pallid sturgeon (A) first feeding larvae (ANOVA, F = 109.131, df =5, P < 0.01, Tukey
post-hoc test), (B) larvae of 20 to 30 mm (Kruskal-Wallis-H, χ2 = 33.457, df = 5, P <
0.01, Dunn-Bonferroni post-hoc test), and (C) larvae of 30 to 40 mm (ANOVA, F =
25.843, df = 5, P < 0.01, Tukey post-hoc test) in 8 day feeding trials in response to
different prey types and a control (i.e., starvation treatment, hatched bar). Different letters
indicate significant differences. ........................................................................................ 40
Figure 2-4: Mean ± SE survival (%) of pallid sturgeon (A) first feeding larvae (Kruskal-
Wallis-H, χ2 = 11.826, df = 4, P = 0.02, Dunn-Bonferroni post-hoc test) and (B) larvae of
20 to 30 mm (Kruskal-Wallis-H, χ2 = 6.495, df = 5, P = 0.17) after 8 day feeding trials in
vii
response to different prey types (open bars) and a control (i.e., starvation treatment,
hatched bars). Different letters indicate significant differences. ...................................... 41
Figure 3-1: Prey selection (V-index and 95 % confidence intervals) by first feeding
pallid sturgeon at 8 density combinations of Chironomidae larvae, zooplankton, and
Ephemeroptera larvae. Prey densities are either high or low and are indicated on top for
individual prey types. Positive selection is indicated by +, neutral selection is indicated
by ±, and negative selection is indicated by –. ................................................................. 77
Figure 3-2: Food habits of first feeding pallid sturgeon. Prey-specific abundance (%) of
Chironomidae larvae, zooplankton and Ephemeroptera larvae is plotted against frequency
of occurrence (%) of each prey type. Diagonal axis from the lower left corner (rare prey
item) to the upper right corner (dominant prey item) indicates prey importance, vertical
axis indicates feeding strategy in terms of generalization (lower part of the graph) and
specialization (upper part of the graph). Plots located in the upper left corner indicate
high consumption of prey types by few individuals and plots in the lower right corner
indicate occasional consumption by many individuals. .................................................... 78
Figure 3-3: Prey selection (V-index and 95 % confidence intervals) by pallid sturgeon
ranging from 20 to 30 mm at 8 density combinations of Chironomidae larvae,
zooplankton, and Ephemeroptera larvae. Prey densities are either high or low and are
indicated on top for individual prey types. Positive selection is indicated by +, neutral
selection is indicated by ±, and negative selection is indicated by –. ............................... 79
Figure 3-4: Food habits of pallid sturgeon ranging from 20 to 30 mm. Prey-specific
abundance (%) of Chironomidae larvae, zooplankton, and Ephemeroptera larvae is
plotted against frequency of occurrence (%) of each prey type. Diagonal axis from the
viii
lower left corner (rare prey item) to the upper right corner (dominant prey item) indicates
prey importance, vertical axis indicates feeding strategy in terms of generalization (lower
part of the graph) and specialization (upper part of the graph). Plots located in the upper
left corner indicate high consumption of prey types by few individuals and plots in the
lower right corner indicate occasional consumption by many individuals. ...................... 80
Figure 3-5: Prey selection (V-index and 95 % confidence intervals) by pallid sturgeon
ranging from 30 to 45 mm at 8 density combinations of Chironomidae larvae,
zooplankton, and Ephemeroptera larvae. Prey densities are either high or low and are
indicated on top for individual prey types. Positive selection is indicated by +, neutral
selection is indicated by ±, and negative selection is indicated by –. ............................... 81
Figure 3-6: Food habits of pallid sturgeon ranging from 30 to 45 mm. Prey-specific
abundance (%) of Chironomidae larvae, zooplankton, and Ephemeroptera larvae is
plotted against frequency of occurrence (%) of each prey type. Diagonal axis from the
lower left corner (rare prey item) to the upper right corner (dominant prey item) indicates
prey importance, vertical axis indicates feeding strategy in terms of generalization (lower
part of the graph) and specialization (upper part of the graph). Plots located in the upper
left corner indicate high consumption of prey types by few individuals and plots in the
lower right corner indicate occasional consumption by many individuals. ...................... 82
Figure 3-7: Prey selection (V-index and 95 % confidence intervals) by pallid sturgeon
ranging from 70 to 200 mm at 4 different density combinations of Chironomidae and
Ephemeroptera larvae. Prey densities are either high or low and are indicated on top for
individual prey types. Positive selection is indicated by +, neutral selection is indicated
by ±, and negative selection is indicated by –. ................................................................. 83
ix
Figure 3-8: Food habits of pallid sturgeon ranging from 70 to 200 mm. Prey-specific
abundance (%) of Chironomidae and Ephemeroptera larvae is plotted against frequency
of occurrence (%) of each prey type. Diagonal axis from the lower left corner (rare prey
item) to the upper right corner (dominant prey item) indicates prey importance, vertical
axis indicates feeding strategy in terms of generalization (lower part of the graph) and
specialization (upper part of the graph). Plots located in the upper left corner indicate
high consumption of prey types by few individuals and plots in the lower right corner
indicate occasional consumption by many individuals. .................................................... 84
Figure 3-9: Prey selection (V-index and 95 % confidence intervals) by pallid sturgeon
ranging from 250 to 450 mm at 4 different density combinations of Chironomidae larvae
and fathead minnow. Prey densities are either high or low and are indicated on top for
individual prey types. Positive selection is indicated by + and negative selection is
indicated by –. ................................................................................................................... 85
Figure 3-10: Food habits of pallid sturgeon ranging from 250 to 450 mm. Prey-specific
abundance (%) of Chironomidae larvae and fathead minnow is plotted against frequency
of occurrence (%) of each prey type. Diagonal axis from the lower left corner (rare prey
item) to the upper right corner (dominant prey item) indicates prey importance, vertical
axis indicates feeding strategy in terms of generalization (lower part of the graph) and
specialization (upper part of the graph). Plots located in the upper left corner indicate
high consumption of prey types by few individuals and plots in the lower right corner
indicate occasional consumption by many individuals. .................................................... 86
Figure 3-11: Prey selection (V-index and 95 % confidence intervals) by pallid sturgeon
ranging from 250 to 450 mm at 4 different density combinations of Chironomidae larvae
x
and Johnny darter. Prey densities are either high or low and are indicated on top for
individual prey types. Positive selection is indicated by + and negative selection is
indicated by –. ................................................................................................................... 87
Figure 3-12: Food habits of pallid sturgeon ranging from 250 to 450 mm. Prey-specific
abundance (%) of Chironomidae larvae and Johnny darter is plotted against frequency of
occurrence (%) of each prey type. Diagonal axis from the lower left corner (rare prey
item) to the upper right corner (dominant prey item) indicates prey importance, vertical
axis indicates feeding strategy in terms of generalization (lower part of the graph) and
specialization (upper part of the graph). Plots located in the upper left corner indicate
high consumption of prey types by few individuals and plots in the lower right corner
indicate occasional consumption by many individuals. .................................................... 88
Figure 3-13: Prey selection (V-index and 95 % confidence intervals) by pallid sturgeon
ranging from 250 to 450 mm at 4 different density combinations of fathead minnow and
Johnny darter. Prey densities are either high or low and are indicated on top for individual
prey types. Both types of fish prey were neutrally selected as indicated by ±. ................ 89
Figure 3-14: Food habits of pallid sturgeon ranging from 250 to 450 mm. Prey-specific
abundance (%) of fathead minnow and Johnny darter is plotted against frequency of
occurrence (%) of each prey type. Diagonal axis from the lower left corner (rare prey
item) to the upper right corner (dominant prey item) indicates prey importance, vertical
axis indicates feeding strategy in terms of generalization (lower part of the graph) and
specialization (upper part of the graph). Plots located in the upper left corner indicate
high consumption of prey types by few individuals and plots in the lower right corner
indicate occasional consumption by many individuals. .................................................... 90
xi
Figure 4-1: Sampling sites at the Lewis and Clark Delta. Red marks represent backwater
sites, orange marks represent Lewis and Clark Lake headwater sites, yellow marks
represent main channel depositional zones, and black marks represent side channel sites.
......................................................................................................................................... 164
Figure 4-2: Mean ± SE growth (mm) of age-0 pallid sturgeon in 4 different habitat types
in the Lewis and Clark Delta (open bars) and the laboratory reference baseline (closed
bar). Habitat types include backwaters, Lewis and Clark Lake headwaters, main channel
depositional zones, and side channels. (ANOVA, F = 1.178, df = 4, P = 0.35). ............ 165
Figure 4-3: Initial (hatched bar) and final mean ± SE energy density (J/g wet weight) of
age-0 pallid sturgeon in 4 different habitat types in the Lewis and Clark Delta (open bars)
and the laboratory reference baseline (closed bar). Habitat types include backwaters,
Lewis and Clark Lake headwaters, main channel depositional zones, and side channels.
(ANOVA, F = 1.985, df = 5, P = 0.10). .......................................................................... 166
xii
LIST OF TABLES
Table 4-1: Physical habitat characteristics for habitat types in the Lewis and Clark Delta.
Habitat types include backwaters, Lewis and Clark Lake headwaters, main channel
depositional zones, and side channels. Presented results are means ± SE. Calculated F-
values refer to ANOVA results. Different letters indicate significant differences.
Significance was assessed at P < 0.1. ............................................................................. 144
Table 4-2: Water quality variables for habitat types in the Lewis and Clark Delta. Habitat
types include backwaters, Lewis and Clark Lake headwaters, main channel depositional
zones, and side channels. Presented results are means ± SE. Calculated F-values refer to
ANOVA results and χ2-values to Kruskal-Wallis-H test results. Different letters indicate
significant differences. Significance was assessed at P < 0.1. ........................................ 145
Table 4-3: Nutrient concentrations for habitat types in the Lewis and Clark Delta. Habitat
types include backwaters, Lewis and Clark Lake headwaters, main channel depositional
zones, and side channels. Presented results are means ± SE. Calculated F-values refer to
ANOVA results and χ2-values to Kruskal-Wallis-H test results. Different letters indicate
significant differences. Significance was assessed at P < 0.1. ........................................ 147
Table 4-4: Zooplankton densities for habitat types in the Lewis and Clark Delta. Habitat
types include backwaters, Lewis and Clark Lake headwaters, main channel depositional
zones, and side channels. Presented results are means ± SE. Calculated F-values refer to
ANOVA results. Different letters indicate significant differences. Significance was
assessed at P < 0.1. .......................................................................................................... 149
xiii
Table 4-5: Benthic invertebrate densities collected with stovepipe samplers for habitat
types in the Lewis and Clark Delta. Habitat types include backwaters, Lewis and Clark
Lake headwaters, main channel depositional zones, and side channels. Presented results
are means ± SE. Calculated F-values refer to ANOVA results and χ2-values to Kruskal-
Wallis-H test results. Different letters indicate significant differences. Significance was
assessed at P < 0.1. .......................................................................................................... 150
Table 4-6: Benthic invertebrate densities collected with D-frame nets for habitat types in
the Lewis and Clark Delta. Habitat types include backwaters, Lewis and Clark Lake
headwaters, main channel depositional zones, and side channels. Presented results are
means ± SE. Calculated F-values refer to ANOVA results. Different letters indicate
significant differences. Significance was assessed at P < 0.1. ........................................ 151
Table 4-7: Physical habitat characteristics at sampling sites in the Lewis and Clark Delta
which supported low and high growth of pallid sturgeon. Presented results are means ±
SE. Calculated t-values refer to t-test results. Significance was assessed at P < 0.1. ..... 152
Table 4-8: Water quality variables at sampling sites in the Lewis and Clark Delta which
supported low and high growth of pallid sturgeon. Presented results are means ± SE.
Calculated t-values refer to t-test results and Z-values refer to Mann-Whitney-U test
results. Significance was assessed at P < 0.1. ................................................................. 153
Table 4-9: Nutrient concentrations at sampling sites in the Lewis and Clark Delta which
supported low and high growth of pallid sturgeon. Presented results are means ± SE.
Calculated t-values refer to t-test results. Significance was assessed at P < 0.1............. 154
Table 4-10: Zooplankton densities at sampling sites in the Lewis and Clark Delta which
supported low and high growth of pallid sturgeon. Presented results are means ± SE.
xiv
Calculated Z-values refer to Mann-Whitney-U test results. Significance was assessed at P
< 0.1. ............................................................................................................................... 155
Table 4-11: Benthic invertebrate densities collected with stovepipe samplers at sampling
sites in the Lewis and Clark Delta which supported low and high growth of pallid
sturgeon. Presented results are means ± SE. Calculated t-values refer to t-test results and
Z-values refer to Mann-Whitney-U test results. Significance was assessed at P < 0.1. . 156
Table 4-12: Benthic invertebrate densities collected with D-frame nets at sampling sites
in the Lewis and Clark Delta which supported low and high growth of pallid sturgeon.
Presented results are means ± SE. Calculated t-values refer to t-test results and Z-values
refer to Mann-Whitney-U test results. Significance was assessed at P < 0.1. ................ 157
Table 4-13: Physical habitat characteristics at sampling sites in the Lewis and Clark
Delta which supported low and high energies density of pallid sturgeon. Presented results
are means ± SE. Calculated t-values refer to t-test results. Significance was assessed at P
< 0.1. ............................................................................................................................... 158
Table 4-14: Water quality variables at sampling sites in the Lewis and Clark Delta which
supported low and high energy densities of pallid sturgeon. Presented results are means ±
SE. Calculated t-values refer to t-test results and Z-values refer to Mann-Whitney-U test
results. Significance was assessed at P < 0.1. ................................................................. 159
Table 4-15: Nutrient concentrations at sampling sites in the Lewis and Clark Delta which
supported low and high energy densities of pallid sturgeon. Presented results are means ±
SE. Calculated T-values refer to t-test results. Significance was assessed at P < 0.1..... 160
Table 4-16: Zooplankton densities at sampling sites in the Lewis and Clark Delta which
supported low and high energy densities of pallid sturgeon. Presented results are means ±
xv
SE. Calculated t-values refer to t-test results and Z-values refer to Mann-Whitney-U test
results. Significance was assessed at P < 0.1. ................................................................. 161
Table 4-17: Benthic invertebrate densities collected with D-frame nets at sampling sites
in the Lewis and Clark Delta which supported low and high energy densities of pallid
sturgeon. Presented results are means ± SE. Calculated t-values refer to t-test results and
Z-values refer to Mann-Whitney-U test results. Significance was assessed at P < 0.1. . 162
Table 4-18: Benthic invertebrate densities collected with D-frame nets at sampling sites
in the Lewis and Clark Delta which supported low and high energy densities of pallid
sturgeon. Presented results are means ± SE. Calculated t-values refer to t-test results and
Z-values refer to Mann-Whitney-U test results. Significance was assessed at P < 0.1. . 163
xvi
ABSTRACT
DETERMINANTS OF GROWTH AND SURVIVAL OF LARVAL PALLID
STURGEON: A COMBINED LABORATORY AND FIELD APPROACH
TOBIAS RAPP
2014
Missouri River modifications caused a loss of shallow water habitats, which was
identified as potential cause for pallid sturgeon Scaphirhynchus albus recruitment failure.
Consequently, recovery effort has focused on habitat restoration, however, ecological
requirements of larval pallid sturgeon are largely unknown. To inform recovery efforts,
we studied the transition from endogenous to exogenous feeding in pallid sturgeon and
quantified prey taxa-specific growth and survival for zooplankton and Chironomidae and
Ephemeroptera larvae in discrete pallid sturgeon size classes (first feeding larvae, 20 to
30 mm, 30 to 40 mm). We quantified pallid sturgeon prey selection offering zooplankton
and Chironomidae and Ephemeroptera larvae to larval pallid sturgeon, Chironomidae and
Ephemeroptera larvae to age-0 juvenile pallid sturgeon, and Chironomidae larvae and
fish prey to age-1 and age-2 juvenile pallid sturgeon. We evaluated four shallow water
habitat types in the Lewis and Clark Delta (i.e., backwaters, side channels, main channel
depositional zones, and Lewis and Clark Lake headwater habitats) regarding their
suitability as nurseries for pallid sturgeon and strived to identify variables that foster
growth and condition (i.e., energy density) of pallid sturgeon.
xvii
We did not observe mixed endogenous and exogenous feeding in pallid sturgeon
and first prey (i.e. zooplankton) was consumed when the yolk sac had been absorbed.
Growth in first feeding larvae was highest for Chironomidae larvae, while in larger larvae
tended to be highest for Ephemeroptera larvae. Survival was high for all prey types in all
size classes (i.e. 88.3 to 100 %). Larval and juvenile pallid sturgeon selected for
Chironomidae larvae throughout all size classes, but consumption of other prey increased
when Chironomidae larvae densities were low. Pallid sturgeon growth, energy density,
and survival did not differ among habitat types in the Lewis and Clark Delta. Sites which
fostered high energy densities had lower velocities, finer substrate, and higher
macrophyte, zooplankton, and benthic invertebrate densities and regression analysis
revealed that pallid sturgeon energy density increased with increasing Ephemeridae and
Caenidae larvae densities.
Overall, our work supports the further creation of shallow water habitat as a tool
for pallid sturgeon recovery. However, the specific habitat type is less important and the
goal of habitat creation should be the increase of primary and secondary productivity,
with focus on macrophytes, zooplankton, and Chironomidae and Ephemeroptera larvae.
1
CHAPTER 1
INTRODUCTION
During the past centuries many rivers have been regulated through damming,
diversion, and channelization in order to meet water and energy demands, mitigate flood
consequences and facilitate navigation (Ward and Stanford 1989, Benke 1990).
Fragmentation and channelization alter the river’s flow regime, which is considered a key
variable, with consequences on geomorphology, water quality (e.g., water temperature),
habitat structure, and ecological functions, collectively threatening the integrity of
riverine ecosystems (Karr 1991, Poff et al. 1997). Many of these consequences were also
reported for the Missouri River, which was extensively modified and is one of the most
regulated rivers within the United States (Hesse et al. 1989, Galat et al. 2005).
Consequently, it was recognized as North America’s most endangered river in 1997,
2001, and 2002 by the organization American Rivers (American Rivers 1997, 2001,
2002).
Historically, the Missouri River was a mosaic of braided, shifting channels with
wide floodplains (Hesse et al. 1989, Galat et al. 2005). Erosion caused high sediment
loads and sediment deposition formed diverse habitats, such as pools, sandbars, islands,
side channels, and backwaters with substantial amounts of woody debris from eroded
riparian and island habitats (Hesse et al. 1989, Galat et al. 1998). The hydrograph was
characterized by two spring pulses in March and in June caused by snow melt and run-off
2
from the Great Plains and the Rocky Mountains, respectively, and declining flow from
summer through winter (Hesse et al. 1989, Galat et al. 1998, 2005).
Missouri River modifications commenced during the 19th century with the
removal of snags to facilitate navigation accompanied by deforestation along the river
banks to power steamboats (Galat et al. 2005). The most significant river modifications
were implemented during the 20th century. The upper Missouri River was impounded by
construction of Fort Peck Dam, Montana in 1937 for water storage to maintain minimum
flows downriver and facilitate navigation in the channelized reach (Galat et al. 2005). In
1944 the Pick-Sloan Plan was enacted and construction of five main-stem dams from
Garrison Dam, North Dakota to Gavins Point Dam, South Dakota commenced in 1946
and was completed in 1963 (Galat et al. 2005). The lower Missouri River was
channelized from Sioux City, Iowa to St. Louis, Missouri to facilitate navigation.
Although channelization started during the early 20th century, the most significant
modifications were implemented under the Missouri River Bank Stabilization and
Navigation Project from 1945 which was completed in 1981 (Galat et al. 2005).
Collectively, Missouri River modifications reduced habitat diversity, disconnected the
Missouri River from its floodplains and resulted in a substantial loss of historically
prevalent shallow water habitats (Hesse and Sheets 1993, Galat et al. 1996, Bowen et al.
2003).
Shallow water habitats including backwaters, side channels, and depositional
zones are important components of large river ecosystems. Shallow water habitats are
generally more heterogeneous than main channel habitats. Lower velocities and longer
3
water retention time decouple the temperature regime from main channel habitats,
facilitate accumulation of organic matter and drift wood, stimulate primary productivity,
and support higher densities of zooplankton and benthic invertebrates, collectively
providing favorable conditions for riverine fishes (Thorp 1992, Thorp and Delong 1994,
Ward and Stanford 1995, Schiemer et al. 2001, 2002). Particularly the significance of
shallow water habitats as nurseries has been emphasized which are rare in large river
ecosystems in absence of retention zones (Schiemer et al. 2001). It was shown that
habitat conditions in shallow water habitats promote growth and survival during the
critical early life history (Schiemer et al. 2001, 2002), during which fish experience high
mortality rates, particularly mediated by starvation, predation, and unsuitable
environmental conditions (Hunter 1981, Houde 1987, Miller et al. 1988, Sogard 1997).
The transition from endogenous to exogenous feeding is generally considered to
be one of the most significant events during early life history of fishes and in many
species is mitigated by a period of mixed feeding; i.e., exogenous food is consumed
before yolk sac reserves are completely absorbed (Hunter 1981, Balon 1986, Houde
1987). Mixed feeding prolongs the start of exclusive exogenous food dependency and
may be advantageous to overcome periods of delayed prey development and poor feeding
efficiency (i.e., the ratio of energy gained from the prey to the total energy costs of food
uptake) of larval fish as feeding ability is compromised owing to functional, anatomical,
physiological and behavioral limitations, that interfere with prey detection, capture, and
ingestion (Hunter 1981, Balon 1986, Houde 1987). Consequently, larval fish can only
consume a small portion of the available prey resources, which renders them particularly
4
vulnerable to starvation when appropriate prey is lacking (Hunter 1981, Balon 1986,
Houde 1987). Starvation can result in poor growth and condition, anatomical and
physiological aberrations, abnormal behavior, and ultimately in death (Kjørsvik et al.
1991, Gisbert and Williot 1997, Gisbert et al. 2004). If deprived of food for extended
time periods at the onset of exogenous feeding, larval fish will approach the “point of no
return” (i.e., effects of food deprivation are irreversible), which is considered to be the
major cause of larval mortality (Blaxter and Hempel 1963, Hunter 1981, Houde 1987).
However, early life stages are also susceptible to indirect lethal consequences of
starvation through size and growth selective mechanisms. Slow growth render early life
stages of fishes more vulnerable to predation at a given age compared to fast-growing
individuals (“bigger-is-better” hypothesis, Miller et al. 1988) and they remain vulnerable
to predation for longer time periods (“stage-duration” hypothesis, Houde 1987).
Furthermore, escape ability is generally compromised in small individuals (Miller et al.
1988). Increased predation vulnerability was also shown for slow growing larvae
compared to fast growing individuals, even if no size differences were apparent, and it
was suspected to be a consequence of poor physiological conditions and associated
behavioral limitations (“growth-selective predation” hypothesis; Takasuka et al. 2003). In
addition to increased predation risk, poor growth and condition may decrease tolerance to
unfavorable environmental conditions. For example, limited energy reserves and higher
mass-specific metabolic rates in smaller individuals may limit the chance of overwinter
survival (Sogard 1997). Thus, food limitation can directly and indirectly increase
mortality rates at which small changes can have pronounced effects on recruitment
(Larkin 1978). As such, availability of quality nursery habitats that provide sufficient
5
suitable prey resources, refuge from predation, and advantageous environmental
condition is essential. The lack of suitable nursery habitats, particularly the loss of
shallow water habitats, is considered to contribute to the decline of several native
Missouri River fishes. One of these species is the pallid sturgeon Scaphirhynchus albus.
The pallid sturgeon is native to the Missouri and Mississippi River drainages and
uses the lower sections of larger tributaries, such as the Yellowstone, Platte and Kansas
rivers (Bailey and Cross 1954). The wild populations of pallid sturgeon in the upper and
middle Missouri River consist of few old individuals and there is no evidence of recent
recruitment (Dryer and Sandvol 1993), although spawning and collection of larval pallid
sturgeon was reported from the Yellowstone River (P. Braaten, personal communication,
United States Geological Survey). Sporadic and limited recruitment may still occur in the
lower Missouri River, but is apparently insufficient to replace aging fish (Keenlyne
1989). Obvious recruitment failure or insufficient recruitment throughout most of its
range resulted in the listing of pallid sturgeon as endangered in 1990 under the
Endangered Species Act and a recovery plan was released in 1993 (Dryer and Sandvol
1993). The pallid sturgeon recovery plan comprises multiple level efforts, including
augmentation through stocking of hatchery-reared individuals, habitat protection and
restoration, and the implementation of research projects vital for recovery of the species
(Dryer and Sandvol 1993). Particular focus is given to the identification of ecological
requirements of early life stages based on limited knowledge and their significance for
recruitment (Wildhaber et al. 2011).
6
To inform pallid sturgeon recovery and habitat restoration efforts we first
conducted a laboratory study to assess whether or not there is a period of mixed
endogenous and exogenous feeding, assessed prey consumption at the transition to
exogenous feeding, and quantified prey taxa-specific growth and survival of larval pallid
sturgeon. Second, in a further laboratory study we quantified prey selection, food habits,
and assessed potential ontogenetic diet shifts in larval and juvenile pallid sturgeon. Third,
to inform habitat restoration efforts we conducted a field study in the Lewis and Clark
Delta of the Missouri River to assess four different shallow water habitat types regarding
their suitability as nurseries for pallid sturgeon. In addition, we measured a suite of
abiotic and biotic variables to identify habitat characteristics that foster pallid sturgeon
growth and condition. Information from this study will also provide important
information for other species in the Missouri River ecosystem.
7
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Gisbert, E., D. B. Conklin, and R. H. Piedrahita. 2004. Effects of delayed first feeding on
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Kjørsvik, E., T. van der Meeren, H. Kryvi, J. Arnfinnson, and P. G. Kvenseth. 1991.
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Takasuka, A., I. Aoki, and I. Mitani. 2003. Evidence of growth-selective predation on
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Simpkins, P. J. Braaten, C. E. Korschgen, and M. J. Mac. 2011. Identifying structural
elements needed for development of a predictive life-history model for pallid and
shovelnose sturgeons. Journal of Applied Ichthyology 27:462-469.
12
CHAPTER II
GROWTH AND SURVIVAL OF LARVAL PALLID STURGEON AT THE ONSET
OF EXOGENOUS FEEDING IN RESPONSE TO DIFFERENT PREY TYPES
ABSTRACT
The transition from endogenous to exogenous feeding is a significant event during
the early life history of fishes. After yolk absorption larval fish are particularly vulnerable
to starvation, which can result in high mortalities with marked consequences on
recruitment. Little is known about the foraging ecology of larval pallid sturgeon
Scaphirhynchus albus, an endangered species endemic to the Missouri and Mississippi
River drainages, which suffers from recruitment failure or insufficient recruitment
throughout its range. We studied the transition from endogenous to exogenous feeding in
pallid sturgeon and quantified prey taxa-specific growth and survival in discrete pallid
sturgeon size classes (first feeding larvae, 20 to 30 mm, 30 to 40 mm). Zooplankton,
Chironomidae and Ephemeroptera larvae as well as a composite diet of all prey types
were offered to pallid sturgeon. A starvation treatment served as a control. First prey
consumption was observed in presence of high zooplankton densities on day 12 post-
hatch, while for other prey types first prey consumption was observed on day 13 post-
hatch. All fish with prey present in the digestive tract had their yolk sac absorbed and no
period of mixed endogenous and exogenous feeding was observed. Growth in first
feeding larvae was highest for Chironomidae larvae, but survival was significantly lower
13
than for zooplankton prey. However, overall survival was high for all prey types and
ranged from 88.3 to 100 %. Growth in larvae of 20 to 30 mm and 30 to 40 mm tended to
be highest when feeding on Ephemeroptera larvae, but differences were only significant
between Ephemeroptera larvae and zooplankton in fish ranging from 30 to 40 mm.
Survival was similar among treatments and ranged from 93.3 % for the starvation
treatment to 100 % for zooplankton and Chironomidae larvae in pallid sturgeon of 20 to
30 mm and approached 100 % for all treatments in pallid sturgeon of 30 to 40 mm. This
study showed that high zooplankton densities at the onset of exogenous feeding may be
advantageous for pallid sturgeon as prey consumption commenced one day earlier than in
other treatments and survival was significantly higher compared to the Chironomidae
larvae treatment. However, the importance of Chironomidae and Ephemeroptera larvae
increases during ontogeny indicated by better growth.
INTRODUCTION
After hatch, larvae of many fishes metabolize yolk sac reserves during the
endogenous feeding period and morphological and physiological adaptations occur and
phenotypical characteristics are developed (Balon 1986, 1999). The duration of the
endogenous feeding period is species-specific, but further subjected to intrinsic (e.g.,
maternal contributions) and extrinsic factors (e.g., temperature, Kamler 2002). The
transition from endogenous to exogenous feeding is generally considered to be one of the
most significant events during early life history of fishes and in many species is mitigated
14
by a period of mixed feeding; i.e., exogenous food is consumed before yolk sac reserves
are completely absorbed (Hunter 1981, Balon 1986, Houde 1987). Mixed feeding
prolongs the start of exclusive exogenous food dependency and may be advantageous to
overcome periods of delayed prey development and poor feeding efficiency of larval fish
(i.e., the ratio of energy gained from the prey to the total energy costs of food uptake)
owing to functional, anatomical, physiological and behavioral limitations, which interfere
with prey detection, capture, and ingestion (Hunter 1981, Balon 1986, Houde 1987).
Consequently, larval fish can only consume a small portion of the available prey
resources, which renders them particularly vulnerable to starvation when appropriate prey
is lacking (Hunter 1981, Balon 1986, Houde 1987). Starvation can result in poor growth
and condition, anatomical and physiological aberrations, abnormal behavior, and
ultimately in death (Kjørsvik et al. 1991, Gisbert and Williot 1997, Gisbert et al. 2004). If
deprived of food for extended time periods at the onset of exogenous feeding, larval fish
will approach the “point of no return” (i.e., effects of food deprivation are irreversible),
which is considered to be the major cause of larval mortality (Blaxter and Hempel 1963,
Hunter 1981, Houde 1987). However, early life stages are also susceptible to indirect
lethal consequences of starvation through size and growth selective mechanisms. Slow
growth render early life stages of fishes more vulnerable to predation at a given age
compared to fast-growing individuals (“bigger-is-better” hypothesis, Miller et al. 1988)
and they remain vulnerable to predation for longer time periods (“stage-duration”
hypothesis, Houde 1987). Furthermore, escape ability is generally compromised in small
individuals (Miller et al. 1988). However, increased predation vulnerability was also
shown for slow growing larvae compared to fast growing individuals, even if no size
15
differences were apparent, and it was suspected to be a consequence of poor
physiological conditions and associated behavioral limitations (“growth-selective
predation” hypothesis; Takasuka et al. 2003). In addition to increased predation risk, poor
growth and condition may decrease tolerance to unfavorable environmental conditions.
Limited energy reserves and higher mass-specific metabolic rates in smaller individuals
may limit the chance of overwinter survival (Sogard 1997). Adaptations in key
characteristics during early life history expand the spectrum of suitable prey resources
triggering progressive diet shifts, which can increase foraging efficiency to meet
increasing energy demands in growing fish (Werner and Gilliam 1984). Thus, the
availability of appropriate prey types during the succession of ontogenetic diet shifts is
essential for growth and survival and can ultimately regulate recruitment for which
starvation and size and growth selective mortality (e.g., predation) during the early life
history are amongst the primary determinants (Hunter 1981, Houde 1987, Miller et al.
1998, Sogard 1997).
Despite the importance of the foraging ecology for recruitment, only limited
information is available on early life stages of pallid sturgeon Scaphirhynchus albus an
endangered species endemic to the Missouri and Mississippi River drainages, which
suffers from obvious recruitment failure or insufficient recruitment throughout most of its
range (Dryer and Sandvol 1993). A lack of information during the ontogenetic foraging
sequence is particularly apparent during the critical life stage when pallid sturgeon
commence exogenous food uptake. Current knowledge is restricted to young-of-the-year
pallid sturgeon, at which Braaten et al. (2012) assessed the diet of six individuals ranging
16
from 48 to 97 mm in length. Fish were collected in the upper Missouri River and prey
was exclusively composed of Diptera larvae and pupae, and Ephemeroptera larvae.
Owing to the similar morphology of pallid sturgeon early life stages to the sympatric
shovelnose sturgeon, S. platorynchus, Sechler et al. (2012, 2013) assessed food habits at
the genus level, Scaphirhynchus spp., which may, however, be rather reflective of the
more common shovelnose sturgeon than the rare pallid sturgeon. Age-0 Scaphirhynchus
spp. in the middle Mississippi River foraged primarily on Chironomidae larvae, Diptera
(including Chironomidae) pupae, and Ephemeroptera larvae. Similarly, Harrison et al.
(2014) observed primarily Chironomidae larvae in the diet of Scaphirhynchus spp.
ranging from 17.66 to 255.50 mm in length in the lower Mississippi River.
Examinations of food habits in natural environments provide important
information on prey composition and selection and allow making inferences on foraging
habitats in individual river reaches. However, it is apparent that investigations are
hampered when the distribution of species which are similar in appearance overlap, as it
is the case for pallid sturgeon and shovelnose sturgeon. Although larval and young-of-
the-year shovelnose sturgeon are insectivores and feed primarily on Diptera and
Ephemeroptera larvae (Braaten et al. 2007), judgment is still out whether or not the
foraging ecology differs between early life stages of pallid sturgeon and shovelnose
sturgeon and thus, investigation at the genus level may result in a loss of information for
both species. In addition, field investigations of rare species’ early life stages are
frequently restricted by numbers of individuals, not allowing for fine-scale size
resolutions. Consolidation of larval and juvenile fish over wide size ranges precludes
17
inferences about the critical early exogenous feeding life stage owing to a potentially
rapid succession of ontogenetic diet shifts during early life history.
This study aimed at investigating the early exogenous feeding life stage of pallid
sturgeon using hatchery-reared progeny in a laboratory setting to, together with previous
work, foster a more holistic understanding of the feeding ecology of pallid sturgeon.
Specifically, the objectives were to assess whether or not there is a period of mixed
endogenous and exogenous feeding, assess prey consumption at the onset of exogenous
feeding, and to quantify prey taxa-specific growth and survival in three discrete size
classes of early exogenous feeding larval pallid sturgeon.
METHODS
Pallid sturgeon yolk sac larvae were obtained on 3 occasions in June and July
2013 from the Gavins Point National Fish Hatchery (Yankton, SD, USA). Fish were
distributed in 3 holding tanks [L × W × H (cm): 110.5 × 110.5 × 40.5] filled with
dechlorinated tap water in a temperature-controlled laboratory. Fish were kept at 17˚C,
analog to the temperature at Gavins Point National Fish Hatchery, and a day:night light
regime of 12:12 h. No filter system was used to avoid entrainment of larval pallid
sturgeon. Partial water exchanges were conducted daily during which dead fish were
removed and water parameter (ammonia: Hach method 8038, nitrite: Hach method 8507)
were measured to maintain adequate water quality according to the Upper Basin Pallid
Sturgeon Propagation Plan (US Fish and Wildlife Service 2005). Fish remained in the
18
holding tanks until they approached the size for each size class tested. For yolk sac
larvae, growth, yolk absorption and onset of exogenous feeding were assessed and
growth and survival was assessed for discrete age or size classes of first feeding larvae,
larvae of 20 to 30mm, and larvae of 30 to 40 mm. Experiments with yolk sac larvae were
initiated 4 days post-hatch, and experiments with first feeding larvae were initiated
shortly before the yolk sac was absorbed (day 11 post-hatch), which was reported to be a
more reliable criterion for the onset of exogenous feeding in Acipenseridae compared to
the evacuation of the melanin plug (Gisbert and Williot 1997, Ghelichi et al. 2010). Yolk
sac and first feeding larvae were not fed prior to the onset of the experiments, while other
size classes were fed a mixed diet of zooplankton and Chironomidae and Ephemeroptera
larvae, which were also used as prey types for the experiments.
Experiments were conducted in 38-L tanks equipped with aeration systems and
illumination at a day:night light regime of 12:12 h. Tanks were filled with 30 L of
dechlorinated tap water at a temperature of 17˚C ± 1 ˚C. Mean water temperature did not
differ significantly over the course of individual trials and between treatments (P > 0.05
for all comparisons). No filter system was used to avoid entrainment of larval pallid
sturgeon and prey. Partial daily water exchanges (10 L) were conducted to ensure
adequate water quality and exclude an influence of water deterioration on growth and
survival rates. Dissolved oxygen and water temperature were monitored daily using a
handheld device (Hach, Loveland, CO, USA, model: HQ40D multiparameter sonde).
Each day, five randomly chosen tanks were analyzed for ammonia and nitrite (ammonia:
Hach method 8038, nitrite: Hach method 8507) to ensure concentrations within an
19
acceptable range according to the Upper Basin Pallid Sturgeon Propagation Plan (US
Fish and Wildlife Service 2005). Due to the lack of information on substrate preferences
of larval pallid sturgeon and potential interactions of prey accessibility and substrate type
no substrate was used. Prey accessibility may differ between substrate types and also may
vary between prey taxa (Ivlev 1961, Levin 1988). For example, accessibility of pelagic
zooplankton may not be influenced by substrate, whereas accessibility of benthic
invertebrates, such as Chironomidae larvae, is decreased in larval pallid sturgeon due to
burying and case building behavior of some Chironomidae larvae (D. Deslaurier,
personal communication, South Dakota State University). Thus, the lack of substrate
ensured that the predetermined prey densities were available to larval pallid sturgeon in
all feeding regimes. Growth, yolk absorption and the onset of exogenous feeding in yolk
sac larvae and prey taxa-specific growth and survival in exogenous feeding larvae were
quantified for zooplankton, Chironomidae and Ephemeroptera larvae, and a treatment
that included all prey types (i.e., composite treatment). A starvation treatment served as
control resulting in n = 5 treatments total. Prey taxa were offered ad libitum, at which
densities for zooplankton were based on water volume and for Chironomidae and
Ephemeroptera larvae were based on tank bottom area. Prey densities were maintained at
a minimum of 50 individuals/L for zooplankton and 950 individuals/m2 for Chironomidae
and Ephemeroptera larvae. Densities were derived from sampling locations in the Fort
Randall Reach of the Missouri River and represent high densities for each prey type
during summer and early fall (benthic invertebrates: Grohs 2008, zooplankton: Rapp
Chapter IV). The composite treatment was conducted at one third of the densities for
each prey type.
20
To assess growth, yolk absorption and the onset of exogenous feeding, yolk sac
larvae were introduced at 70 per tank four days post-hatch and experiments continued
through day 13 post-hatch. Each day three larvae were sampled per tank to assess growth,
yolk volume and examine the digestive tract for prey, at which individual larvae from
each tank were treated as sub-samples. For assessment of growth and survival in first
feeding larvae and larvae of 20 to 30 mm, 10 fish were placed in each tank at the
beginning of the experiment and individual fish were treated as sub-samples. One fish
was used per tank for assessment of growth and survival in larvae of 30 to 40 mm. Initial
size for each size class was based on 10 randomly chosen fish. Prey taxa-specific growth
and survival experiments were conducted over 8 days during which dead larvae were
removed and counted daily to quantify survival. All sampled fish were euthanized and
preserved in 10 % formalin solution until analysis. Each treatment was replicated 6 times.
All measurements (larval total length, yolk length and width) were conducted to the
nearest 0.01 mm using a dissecting scope (Olympus America, Mellville, NY, USA,
model: SZH 10) with appropriate software (Olympus America, Mellville, NY, USA,
model: DP2-BSW, version: 2.2). Yolk volume was calculated based on a prolate spheroid
shape (Blaxter and Hempel 1963).
Repeated measures analysis of variance (ANOVA) was used to compare daily
growth and yolk volume in trials with yolk sac larvae. In other size classes fish length
was assessed at the end of the trials and compared with one-way ANOVAs followed by a
Tukey post-hoc test in significant models. Compliance with assumptions for parametric
tests was tested with Kolmogorov-Smirnov test for normality, Levene’s test for
21
homogeneity of variances, and Mauchley’s test for sphericity in repeated measures
ANOVAs. A Kruskal-Wallis-H test was used if assumption of normal distribution was
violated followed by a Dunn-Bonferroni post-hoc test in significant models. Proportion
data was compared among treatment groups using a Kruskal-Wallis-H test followed by a
Dunn-Bonferroni post-hoc test in significant models as arcsine square root
transformations did not satisfy assumptions of normal distribution. Significance was
judged at α < 0.05. All results are presented as non-transformed values to facilitate
interpretation. Statistical analyses were conducted using the software package SPSS 21.0
(IBM, Armonk, NY, USA).
RESULTS
Pallid sturgeon growth and yolk volume did not differ between treatments
(growth: repeated measures ANOVA, treatment effect: F = 1.040, df = 4, P = 0.41, yolk
volume: repeated measures ANOVA, treatment effect: F = 0.130, df = 4, P = 0.97) and
consequently further investigations were pooled for all treatments (Figure 1). Yolk was
present in 93.9 %, 4.4 %, and 2.4 % of pallid sturgeon at day 11, day 12, and day 13 post-
hatch, respectively. First feeding was observed 12 days post-hatch at a mean ± SE total
length of 18.01 ± 0.08 mm, at which mean ± SE 16.5 ± 7.4 % of pallid sturgeon feeding
on zooplankton consumed prey, while prey ingestion was not observed in other
treatments (Kruskal-Wallis-H, χ2 = 9.350, df = 3, P = 0.03; Figure 2 A). All fish with prey
present in the digestive tract had their yolk absorbed. At day 13 post-hatch and a mean
22
total length of 18.27 ± 0.1 mm feeding was observed in all treatment groups except for
the starvation treatment and mean ± SE 41.7 ± 5.7 %, 41.7 ± 16.0 %, 38.9 ± 13.4 %, and
27.8 ± 5.6 % of pallid sturgeon offered zooplankton, Ephemeroptera larvae,
Chironomidae larvae, and the composite diet of all prey types ingested prey (Kruskal-
Wallis-H, χ2 = 1.724, df = 3, P = 0.63; Figure 2 B).
Mean ± SE initial total length of first feeding larvae was 18.17 ± 0.13 mm.
Despite no food present in the starvation treatment and fish not being fed prior to the
experiment, final mean larval pallid sturgeon length was 2.03 mm larger than the mean
length at the start of the experiment. During the first week of exogenous feeding, pallid
sturgeon grew significantly larger when feeding on Chironomidae larvae compared to
other prey types or a composite diet of all prey types. (ANOVA, F = 109.131, df =5, P <
0.01, Tukey post-hoc test; Figure 3 A). However, pallid sturgeon survival was
significantly lower when feeding on Chironomidae larvae (mean ± SE: 88.3 ± 1.7 %)
compared to when feeding zooplankton (100 %), while similar to all other prey types and
the starvation treatment (starvation, mean ± SE: 93.3 ± 3.3 %; Ephemeroptera larvae,
mean ± SE: 96.7 ± 2.1 %; composite treatment, mean ± SE: 88.3 ± 4.0 %; Kruskal-
Wallis-H, χ2 = 11.826, df = 4, P = 0.02, Dunn-Bonferroni post-hoc test; Figure 4 A).
Mean ± SE initial total length in the 20 to 30 mm size class was 22.2 ± 0.34 mm
and was similar in the starvation treatment at the end of the feeding trial. Growth was
highest in fish that were offered Ephemeroptera larvae or a combination of all prey types
in lower densities (i.e., composite treatment), while tended to be lower in fish that were
offered Chironomidae larvae and zooplankton, although differences were not significant.
23
(Kruskal-Wallis-H, χ2 = 33.457, df = 5, P < 0.01, Dunn-Bonferroni post-hoc test; Figure 3
B). Survival did not differ significantly between treatment groups (Kruskal-Wallis-H, χ2 =
6.495, df = 5, P = 0.17; Figure 4 B).
Mean ± SE initial total length in the 30 to 40 mm size class was 33.29 ± 0.72 mm
and was similar in the starvation treatment at the end of the feeding trial. Fish that were
offered Ephemeroptera larvae grew significantly larger than fish feeding on zooplankton,
while performance of Chironomidae larvae and the composite treatment were
intermediate and not different from either the Ephemeroptera larvae or zooplankton
treatment (ANOVA, F = 25.843, df = 5, P < 0.01, Tukey post-hoc test; Figure 3 C). No
mortalities were observed in any treatment.
DISCUSSION
Pallid sturgeon yolk volume and growth did not differ during the endogenous
feeding period in response to different prey types and first prey was observed in the
digestive tract when the yolk sac was absorbed, which has previously been reported for
other Acipenseridae (Buckley and Kynard 1981, Wegner et al. 2009, Gisbert and Williot
1997, Ghelichi et al. 2010). However, Gisbert et al. (1998) observed in a histological
study remains of microscopic yolk granules in the stomach while first food was
consumed and concluded that a brief period of mixed endogenous and exogenous feeding
occurs in Siberian sturgeon Acipenser baeri. Such fine scale analysis was not feasible in
the context of our study and we only assessed external yolk (Snyder 2002). Thus, the
24
presence of microscopic internal yolk cannot be completely ruled out. Yet, presence of
the melanin plug, a product of yolk digestion, in yolk sac larvae with empty digestive
tracts (day 11 post-hatch) and the simultaneous presence of the melanin plug and prey in
some individuals after the yolk was depleted (days 12 and 13 post-hatch) support the
notion that the melanin plug was expelled with the first feces and no prey was consumed
by pallid sturgeon prior to external yolk absorption (Gisbert and Williot 1997, Ghelichi et
al. 2010). The absence of a pronounced mixed endogenous and exogenous feeding in
pallid sturgeon differs markedly from Chinese sturgeon A. sinensis, which incorporated
exogenous food at day 8 post-hatch while the yolk sac was not depleted until day 10 post-
hatch (Chai et al. 2011). One reason for differences between Acipenseridae at the onset of
exogenous feeding may be related to their life history strategy. Pallid sturgeon cease drift
and settle in nursery habitats when the yolk sac is absorbed (Kynard et al. 2007), while
Chinese sturgeon settle in nurseries prior to complete yolk sac absorption (Zhuang et al.
2002) where they may resume feeding while yolk is still present. Thus, it seems plausible
that the onset of exogenous food is inherently linked to the migration behavior or habitat
switch during the larval period. Similarly, green sturgeon A. medirostris, Atlantic
sturgeon A. oxyrinchus oxyrinchus and shortnose sturgeon A. brevirostrum do not
disperse during the endogenous feeding stage, emerge from the substrate once the yolk
sac is depleted, and commence larval drift which is interrupted by foraging bouts (Kynard
and Horgan 2002, Kynard et al. 2005)
On day 12 post-hatch about 94 % of larval pallid sturgeon had their yolk
absorbed, which coincided with exposure to between 187 to 204 CTU. Although the
25
exact CTU could not be assessed as larvae were only sampled every 24 h, the observed
range is similar to that of 198 to 205 CTU which was reported by Kynard et al. (2007) for
similar water temperatures. Prey consumption on day 12 post-hatch was exclusively
observed in presence of high zooplankton densities (i.e., zooplankton treatment), while
no evidence for exogenous feeding was observed for other prey types or if zooplankton
was only present in low densities (i.e., composite treatment) until day 13 post-hatch. A
potential reason may be related to the prey densities used in the feeding trials, which
resulted in higher absolute numbers for zooplankton in individual tanks (minimum 1500
individuals/tank) than for benthic invertebrates (minimum 123 individuals/tank) or the
composite treatment (minimum 500 individuals/tank for zooplankton and 41
individuals/tank for each benthic invertebrate prey type). Thus, higher numbers of prey
may increase encounter rates and subsequently prey consumption (Blaxter 1986). Prey
size was likely not the reason for the delayed start of feeding as larvae were not
significantly larger on day 13 post-hatch compared to day 12 post-hatch. We were not
able to identify ingested zooplankton taxa in this study due to the advanced state of
digestion. However, Rapp (Chapter III) observed primarily Daphnia spp. in the digestive
tract of larval pallid sturgeon feeding on zooplankton in short-term prey selection trials.
Similarly, Daphnia spp. were the primary zooplankton taxa consumed by Persian
sturgeon A. persicus (Amirkolaie 2009). Ingested prey taxa could not be identified in the
composite treatment. The complete absence of benthic invertebrate structures in digestive
tracts, which were found in Chironomidae and Ephemeroptera larvae treatments,
however, suggest that larval pallid sturgeon fed primarily on zooplankton. This could
again be related to numbers of each prey type in the composite treatment as Rapp
26
(Chapter III) observed opportunistic feeding behavior in prey selection trials with larval
pallid sturgeon.
In larger size classes (i.e., first feeding larvae, 20 to 30 mm and 30 to 40 mm)
growth differed among prey types and was highest for benthic invertebrates. Increasing
importance of benthic invertebrates compared to zooplankton during ontogeny may be
attributed to the transition to demersal life stage once larval pallid sturgeon settle in
nursery habitats. Similarly, Buckley and Kynard (1981) observed a switch from
zooplankton to benthic prey during the first weeks of exogenous feeding in shortnose
sturgeon and Amirkolaie (2009) reported a decrease of zooplankton and an increase of
Chironomidae larvae in the diet of larval Persian sturgeon during ontogeny. Furthermore,
field studies with age-0 pallid sturgeon and the closely related shovelnose sturgeon
observed primarily Chironomidae larvae and pupae and Ephemeroptera larvae in the diets
(Sechler et al. 2012, 2013, Braaten et al. 2007, 2012, Harrison et al. 2014). Over an 8 day
period, first feeding larvae grew largest when high densities of Chironomidae larvae were
provided, which may be related to differences in feeding efficiency between prey types
(i.e., the ratio of energy gained from the prey to the total energy costs of food uptake).
Larval pallid sturgeon have poor swimming ability (D. Deslaurier personal
communication, South Dakota State University). The behavioral limitations likely have
direct consequences on capture efficiency and favor sluggish prey, such as Chironomidae
larvae, compared to agile prey, such as Ephemeroptera larvae, and result in higher
feeding efficiency for Chironomidae larvae. Lower capture efficiency for Ephemeroptera
larvae compared Chironomidae larvae or other slow benthic invertebrate taxa has been
27
shown for age-0 pallid sturgeon (Rapp Chapter II) and Adriatic sturgeon, A. naccarii
(Soriguer et al. 2002). Observed growth differences between the Chironomidae larvae
treatment and the composite treatment in first feeding larvae suggest again that there may
have been a prey density effect. Despite better growth, survival was significantly lower
for Chironomidae larvae compared to high zooplankton densities, for which 100 %
survival was observed, which may originate in the earlier onset of exogenous feeding as
described before. The experiments with first feeding larvae commenced about one day
before complete yolk absorption, and may indicate that availability of zooplankton
mitigates the transition to exogenous feeding. Although Acipenseridae are generally less
sensitive to food deprivation compared to other species, a delay in exogenous food uptake
of only few days can significantly increase mortality rates (Gisbert and Williot 1997,
Hardy and Litvak 2004). The onset of the experiments with first feeding larvae while
small quantities of yolk were present may also explain the significant growth in
starvation treatment. Growth in the 20 to 30 mm and 30 to 40 mm size classes tended to
be higher for Ephemeroptera larvae compared to Chironomidae larvae, although
differences were not significant. During early ontogeny, larvae undergo rapid successions
of adaptations which improve capture efficiency (Nunn et. al 2012). These adaptations
may in conjunction with higher energy densities of Ephemeroptera larvae compared to
Chironomidae larvae (Cummins and Wuycheck 1971) increase feeding efficiency.
Survival rates in trials with larvae ranging from 20 to 30 mm and 30 to 40 mm were high
and approached 100 % for pallid sturgeon larvae of 30 to 40 mm, which supports the
notion that mortality decreases with increasing fish size as is observed in many other
species (Hunter 1981, Houde 1987).
28
Information on the feeding ecology provides important implications for the
understanding and recovery of pallid sturgeon. During drift, large-scale patterns of larval
distribution are primarily determined by hydrodynamic properties and river morphology
and only fine-scale spatial patterns can be regulated via active movement (Bradburry and
Snelgrove 2001, Schiemer et al. 2002). Our results suggest that pallid sturgeon do not
consume prey during the planktonic life stages and once drift ceases, are immediately
dependent on quality and quantity of exogenous prey. The lack of a pronounced mixed
endogenous and exogenous feeding period, which is considered to mitigate the critical
transition to exclusive exogenous food dependency, renders larval pallid sturgeon
particularly vulnerable to starvation if appropriate prey is rare (Hunter 1981, Balon 1986,
Houde 1987) and emphasizes the importance of quality nursery habitats within the drift
distance of pallid sturgeon larvae in the Missouri and Mississippi rivers. Although there
is plasticity in first prey and pallid sturgeon incorporated all prey types in their diet once
the yolk sac was absorbed our results suggest that high zooplankton densities are
advantageous, as a portion of pallid sturgeon started to consume prey one day earlier, and
it may be possible that the slight, yet significant, differences in survival during the first
feeding trials are a result of the successful transition to exogenous food uptake.
Zooplankton represents important prey for most larval fishes and is an important diet
component for over 60 fishes in the Missouri River at least during part of their life history
(Wildhaber et al. 2011). Similar to our observations with pallid sturgeon, zooplankton
was reported as first prey in shortnose sturgeon after yolk sac absorption (Buckley and
Kynard 1981). Also Persian sturgeon fry fed primarily on Daphnia spp. and
Chironomidae larvae, at which Daphnia spp. consumption decreased during ontogeny,
29
whereas Chironomidae larvae consumption increased (Amirkolaie 2009). Although we
were not able to identify ingested zooplankton taxa, Rapp (Chapter III) observed
primarily Daphnia spp. in digestive tracts of larval pallid sturgeon during prey selection
experiments. In large rivers, higher densities of Daphnia spp. and other zooplankton taxa
occur in inshore habitats and their significance as nurseries for larval and juvenile fish
has been emphasized (Keckeis et al. 1997, Schiemer et al. 2001, Schiemer et al. 2002).
We demonstrated that after successful transition to exogenous feeding, benthic
invertebrates such as Chironomidae and Ephemeroptera larvae are important diet
components. Growth in first feeding larvae was enhanced in presence of high
Chironomidae larvae densities, potentially due to their sluggish behavior. In pallid
sturgeon from 20 to 30 and 30 to 40 mm growth tended to be greater in presence of high
Ephemeroptera larvae densities, potentially due to adaptations in key characteristics
during ontogeny facilitating prey capture or higher energy density of Ephemeroptera
larvae.
We caution that this study was conducted at ad libitum feeding rates using prey
densities derived from highest densities observed during summer and early fall in the Fort
Randall Reach of the middle Missouri River (benthic invertebrates: Grohs 2008,
zooplankton: Rapp Chapter IV) and no substrate was used to avoid interactions of
substrate type and prey availability. Thus, all benthic invertebrates provided were
available to pallid sturgeon larvae. However, encasement with fine sediment or burying
in sediment can decrease predation success of pallid sturgeon larvae on benthic
invertebrates (e.g., Chironomidae larvae, D. Deslaurier personal communication, South
30
Dakota State University). Therefore, it is crucial in habitat evaluations to assess actually
available benthic invertebrates for larval pallid sturgeon as some sampling gear such as,
for example, grab samplers may severely overestimate the densities of available benthic
invertebrate prey by including buried individuals. The composite treatment showed that
lower prey densities do not provide the same advantages compared to high densities as
neither did the transition to exogenous prey occur as early as in the pure zooplankton
treatment, nor did first feeding larvae grow as well as in the pure Chironomidae larvae
treatment. As such, availability of appropriate prey types during ontogeny is essential and
a mismatch between appearance of larval pallid sturgeon in nursery habitats and
availability of quantity and quality of prey could decrease growth and increase mortality
either directly through starvation or through size and growth selective mechanisms (e.g.,
predation), at which even minor changes can have marked consequences on recruitment
(Larkin 1978).
ACKNOWLEDGEMENTS
Funding for this study was provided by the US Army Corps of Engineers. We
thank the hatchery personnel at Gavins Point National Fish Hatchery for providing pallid
sturgeon larvae and Jason Augspurger, Tanner Brower, and Tyler Trimpe for laboratory
assistance.
31
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38
Days post-hatch (cumulative thermal units)
4 6 8 10 12 14
Tota
l le
ngth
(m
m)
12
13
14
15
16
17
18
19
Yolk
volu
me (
mm
3)
0
1
2
3
4
5
6
7
(68) (102) (136) (170) (204) (238)
Z C E
Figure 2-1: Mean ± SE total length (mm; open circles) and mean ± SE yolk volume
(mm3; closed circles) of larval pallid sturgeon from day 5 to 13 post-hatch. Physiological
age, expressed as cumulative thermal units, is given in brackets. Differences between
prey types were not significant and presented data is pooled over all treatments (growth:
repeated measures ANOVA, treatment effect: F = 1.040, df = 4, P = 0.41, yolk volume:
repeated measures ANOVA, treatment effect: F = 0.130, df = 4, P = 0.97). Arrows
indicate the first ingestion of the different prey types (Z = zooplankton, C =
Chironomidae larvae, E = Ephemeroptera larvae).
39
Feed
ing f
ish
(%
)
0
5
10
15
20
25
30
Prey type
0
10
20
30
40
50
60
70
Zoopla
nkton
Ephem
erop
tera
Chir
onom
idae
Com
posite
A
B
Figure 2-2: Mean ± SE percentage of feeding pallid sturgeon in response to different
prey types at (A) day 12 post-hatch (Kruskal-Wallis-H, χ2 = 9.350, df = 3, P = 0.03) and
(B) day 13 post-hatch (Kruskal-Wallis-H, χ2 = 1.724, df = 3, P = 0.63).
40
Prey type
0
5
10
15
20
25
ab
c c cd
Prey type
0
10
20
30
40
50
60
Start
Starv
atio
n
Zoopla
nkton
Ephem
erop
tera
Chir
onom
idae
Com
posite
a a
bbc
bcc
To
tal
len
gth
(m
m)
0
5
10
15
20
25
30
35
a a
ab
bab
b
a a
bbc
bc
c
A
B
C
Figure 2-3: Initial (closed bar) and final (open bar) mean ± SE total length (mm) of
pallid sturgeon (A) first feeding larvae (ANOVA, F = 109.131, df =5, P < 0.01, Tukey
post-hoc test), (B) larvae of 20 to 30 mm (Kruskal-Wallis-H, χ2 = 33.457, df = 5, P <
0.01, Dunn-Bonferroni post-hoc test), and (C) larvae of 30 to 40 mm (ANOVA, F =
25.843, df = 5, P < 0.01, Tukey post-hoc test) in 8 day feeding trials in response to
different prey types and a control (i.e., starvation treatment, hatched bar). Different letters
indicate significant differences.
41
Prey type
Su
rv
iva
l (%
)
0
20
40
60
80
100 abb
a abab
Prey type
0
20
40
60
80
100
Starv
atio
n
Zoopla
nkton
Ephem
erop
tera
Chir
onom
idae
Com
posite
A
B
Figure 2-4: Mean ± SE survival (%) of pallid sturgeon (A) first feeding larvae (Kruskal-
Wallis-H, χ2 = 11.826, df = 4, P = 0.02, Dunn-Bonferroni post-hoc test) and (B) larvae of
20 to 30 mm (Kruskal-Wallis-H, χ2 = 6.495, df = 5, P = 0.17) after 8 day feeding trials in
response to different prey types (open bars) and a control (i.e., starvation treatment,
hatched bars). Different letters indicate significant differences.
42
CHAPTER III
ONTOGENY OF THE FEEDING ECOLOGY IN PALLID STURGEON: SEQUENCE
OF PREY SELECTION AND FOOD HABITS FROM FIRST FEEDING LARVAE TO
AGE-2 JUVENILE FISH
ABSTRACT
The foraging ecology of fishes provides vital information for effective population and
community management with important implications for habitat conservation and
restoration. Considerable attention has been paid to assess diet composition and food
habits of juvenile and adult pallid sturgeon Scaphirhynchus albus in field studies, but
information on larval life stages is lacking. Furthermore no experimental studies on prey
selection and feeding behavior are available for juvenile fish. Thus, we examined larval
pallid sturgeon prey selection for three discrete size classes (first feeding, 20 to 30 mm,
30 to 45 mm) using zooplankton and Chironomidae and Ephemeroptera larvae as prey. In
addition, we assessed prey selection and feeding behavior for discrete size classes of
juvenile pallid sturgeon. Chironomidae and Ephemeroptera larvae were used as prey
types for age-0 juvenile fish ranging from 70 to 200 mm larvae and two types of fish prey
(fathead minnow, Pimephales promelas, and Johnny darter, Etheostoma nigrum) and
Chironomidae larvae were used as prey for age-1 and age-2 juvenile pallid sturgeon
ranging from 250 to 450 mm. Prey selection was assessed in low and high prey density
combinations. Larval pallid sturgeon selected positively for Chironomidae larvae.
43
However, when Chironomidae larvae were available in low densities and Ephemeroptera
were available in high densities pallid sturgeon selected positively for Ephemeroptera
larvae. Zooplankton, particularly Daphnia spp., was frequently consumed by larval pallid
sturgeon, however selection was negative. Juvenile fish ranging from 70 to 200 mm
selected positively for Chironomidae larvae, but consumption of Ephemeroptera larvae
increased when available in high densities and Chironomidae larvae were available in
low densities. Pallid sturgeon ranging from 250 to 450 mm selected positively for
Chironomidae larvae and negatively for both types of fish prey at all prey density
combinations. Capture efficiency and number of feeding attempts were higher for
Chironomidae larvae than for Ephemeroptera larvae or fish prey. The results indicate that
Chironomidae larvae are the selected prey type by larval and juvenile pallid sturgeon, but
consumption of other prey types increases when Chironomidae larvae are rare.
Furthermore our results suggest that Daphnia spp. can contribute to the diet of larval
pallid sturgeon, while other zooplankton taxa are rarely consumed.
INTRODUCTION
The foraging ecology of fishes provides vital information for the understanding of
individuals and their interactions at the population and community level through
competition and predation and contributes to the understanding of distribution patterns
and habitat use (Nunn et al. 2012). Thus, information on foraging ecology provides
important implications for effective population, community and habitat management, and
44
conservation strategies (Nunn et al. 2012). Understanding of the foraging ecology is of
particular significance for early life stages, which represent a bottleneck in many fish
populations at which even minor changes in survival can have pronounced effects on
recruitment (Larkin 1978). Larval fish are subjected to functional, anatomical,
physiological and behavioral limitations which interfere with prey detection, capture, and
ingestion (Hunter 1981, Balon 1986, Houde 1987). Consequently early life stages can
only consume a small portion of the available prey items, which renders them particularly
vulnerable to starvation when suitable prey resources are lacking (Hunter 1981, Balon
1986, Houde 1987). Even short periods of starvation at the onset of exogenous feeding
can result in poor growth and condition, anatomical and physiological aberrations,
abnormal behavior, and ultimately death (Kjørsvik et al. 1991, Gisbert and Williot 1997,
Gisbert et al. 2004). Starvation may either cause mortalities directly or it may mediate
mortalities, for example through size and growth selective mechanisms. Slow growth
renders early life stages of fishes more vulnerable to predation at a given age compared to
fast-growing individuals (“bigger-is-better” hypothesis, Miller et al. 1988) and they
remain vulnerable to predation for longer time periods (“stage-duration” hypothesis,
Houde 1987). Furthermore, escape probability is generally compromised in small
individuals (Miller et al. 1988). However, increased predation vulnerability was also
shown for slow growing larvae compared to fast growing individuals, even if no size
differences were apparent, and it was suspected to be a consequence of poor
physiological conditions and associated behavioral limitations (“growth-selective
predation” hypothesis; Takasuka et al. 2003). In addition to increased predation risk, poor
growth and condition may decrease tolerance to unfavorable environmental conditions.
45
For example, limited energy reserves and higher mass-specific metabolic rates in smaller
individuals may limit the chance of overwinter survival (Sogard 1997). Both, starvation
and predation are considered to be among the primary causes of mortality during early
life history and can result in pronounced effects on recruitment (Hunter 1981, Houde
1987, Miller et al. 1988).
Adaptations in key characteristics generally expand the spectrum of suitable prey
resources and can ultimately trigger progressive diet shifts either towards prey of the
same type (e.g., larger zooplankton sizes or taxa) or towards prey of a different type (e.g.,
diet shifts from zooplankton to benthic invertebrates), which are, in some species,
accompanied by habitat shifts (Werner and Gilliam 1984, Balon 1986, Nunn et al. 2012).
Diet shifts are assumed to prevent bottlenecks resulting from intraspecific competition
(Werner and Gilliam 1984, Balon 1986, Nunn et al. 2012) and increase foraging
efficiency (i.e., the ratio of energy gained from the prey to the total energy costs of food
uptake) to meet increasing energy demands in growing fish (Werner and Gilliam 1984,
Keast 1985). Thus, progressive diet shifts can benefit growth and, in turn, decrease size
and growth selective mortalities. Age at which ontogenetic diet shifts occur is dependent
on a variety of intrinsic factors (Wainwright and Richard 1995, Mittelbach and Persson
1998), but also motivated by extrinsic factors, which can either be biotic factors, such as
available prey taxa and prey sizes (Hanson and Wahl 1981), competition (Persson and
Greenberg 1990), and predation risk (Werner and Hall 1988) or abiotic factors (i.e.,
environmental conditions, Olson 1996). As a result, biotic and abiotic factors can delay or
46
interrupt ontogenetic diet shifts of fishes and thus, the realized diet represents a trade-off
between intrinsic and extrinsic factors.
In many piscivorous species more than one ontogenetic diet shift is common at
which the diet typically progresses from zooplankton to benthic invertebrates to fish prey
(Keast 1985, Mittelbach and Persson 1998, Nunn et al. 2012). However there is great
variation in age when diet shifts occur, which is particularly apparent for the final diet
shift to fish prey (Keast 1985, Mittelbach and Persson 1998, Juanes et al. 2001). Based on
their ontogenetic food habits, Keast (1985) broadly grouped piscivorous fishes into
primary or specialized piscivores, secondary or opportunistic piscivores and fish that only
feed occasionally on larvae or small fishes. Primary piscivores, such as pike Esox esox,
largemouth bass Micropterus salmoides, or walleye Sander vitreus generally switch to
fish prey during the first summer and are structurally well adapted to a piscivorous life
style (Keast 1985, Mittelbach and Persson 1998, Graeb et al. 2005). Secondary piscivores
switch to fish prey later in life and are lacking specialized adaptation for a piscivorous
life style except for a large gape size. Secondary piscivores gradually switch to larger
prey during ontogeny and eventually incorporate fish in the diet to meet energetic
requirements, but other prey types remain integral diet components (Keast 1985,
Mittelbach and Persson 1998). This includes species such as yellow perch Perca
flavescens or rock bass Ambloplites rupestris (Keast 1985, Graeb et al. 2005).
Prey selection can involve passive and active choices by the predator and several
passive (i.e., mechanistic) and active (i.e., functional) selection models have been
proposed to describe food habits and ontogenetic diet shifts in fish. Mechanistic models
47
explain how and when fish detect their prey and comprise several aspects of the feeding
sequence, such as the encounter situation, detection, attack, capture and ingestion of prey
(Holling 1959). Selection can occur during each step of the predator-prey interaction and
is based on perception of prey, including size and shape, coloration and visual contrast,
and prey behavior. Functional models propose a general theory of active prey choice and
the balance between costs and rewards. This theory of optimal foraging is subjected to
two basic assumptions: First, predators select for prey that yields more energy per unit
handling time, probability of capture, and digestive time, although the impact of digestive
time on prey ranking is controversial (Stephens and Krebs 1986, Kaiser et al. 1992, Sih
and Christensen 2001). Second, selection towards energetically more profitable prey will
increase with increasing abundance of this prey type in the environment and consequently
less profitable prey will be dropped from the diet (Stephens and Krebs 1986, Sih and
Christensen 2001). Conversely, energetically less profitable prey will increase in the diet,
when more profitable prey becomes scarce (Stephens and Krebs 1986, Sih and
Christensen 2001). Juanes (1994) proposed that prey selection in piscivorous fishes is a
passive rather than an active process, while other authors suspected active selection, for
example for pikeperch Sander lucioperca and the closely related walleye (Einfalt and
Wahl 1997, Turesson et al. 2002).
Despite the importance for recruitment and its implications for effective
management and conservation, only limited information is available on the foraging
ecology of early life stages of pallid sturgeon Scaphirhynchus albus an endangered
species endemic to the Missouri and Mississippi River drainages (Dryer and Sandvol
48
1993), and information on larval life stages is lacking. Current information on early life
stages is limited to a field study by Braaten et al. (2012) who assessed diet composition in
six individuals ranging from 48 to 97 mm, at which the diet was composed of Diptera
larvae and pupae and Ephemeroptera larvae. Due to similarity in appearance and
distribution overlap of pallid sturgeon and the closely related shovelnose sturgeon S.
platorynchus, Sechler et al. (2012, 2013) assessed food habits at the genus level,
Scaphirhynchus spp., which may however be more reflective of the more common
shovelnose sturgeon. In both studies, Chironomidae larvae and Diptera (including
Chironomidae) pupae as well as Ephemeroptera larvae were frequently observed prey
items (Sechler et al. 2012, 2013). Similarly, Harrison et al. (2014) reported mainly
Chironomidae larvae in the diet of age-0 Scaphirhynchus spp. Studies on larger juvenile
and adult fish suggest that pallid sturgeon undergo an ontogenetic diet shift from benthic
invertebrates to fish prey during the juvenile life stage (Gerrity et al. 2006). However,
diet composition in field studies varied seasonally (Wanner et al. 2007) and between
sampling locations (Carlson et al. 1985, Gerrity et al. 2006, Wanner et al. 2007, Hoover
et al. 2007, Grohs et al. 2009) and may be influenced by prey availability (Grohs et al.
2009). Thus, the realized diet of pallid sturgeon in field studies may represent a trade-off
between opposing effects of intrinsic (e.g., gape size; Mittelbach and Persson 1988) and
extrinsic factors (e.g., prey availability, competition, predation risk, or environmental
conditions; Hanson and Wahl 1981, Werner and Hall 1988, Persson and Greenberg 1990,
Olson 1996).
49
So far, information on prey selection and ontogenetic diet shifts in larval pallid
sturgeon is lacking. In addition, no study has examined prey selection in juvenile pallid
sturgeon under controlled conditions to exclude an influence of prey availability on
selection patterns. Thus, we conducted a laboratory study to assess prey selection, food
habits, and potential ontogenetic diet shifts in discrete size classes ranging from first
feeding larvae to age-2 juvenile pallid sturgeon of 450 mm without interference of
potentially opposing effects.
METHODS
Prey selection of larval pallid sturgeon
Pallid sturgeon yolk sac larvae were obtained from the Gavins Point National Fish
Hatchery (Yankton, South Dakota, USA) in June 2013. Fish were distributed in 3 holding
tanks [L × W × H (cm): 110.5 × 110.5 × 40.5] filled with dechlorinated tap water in a
temperature-controlled laboratory at South Dakota State University. Fish were kept at
17˚C, similar to the temperature at Gavins Point National Fish Hatchery, and a day:night
light regime of 12:12 h. No filter system was used to avoid entrainment of larval pallid
sturgeon. Partial water exchanges were conducted daily during which dead fish were
removed and water quality parameters (ammonia: Hach method 8038, nitrite: Hach
method 8507) were measured to maintain adequate water quality according to the Upper
Basin Pallid Sturgeon Propagation Plan (US Fish and Wildlife Service 2005). Fish
remained in the holding tanks until they approached the respective size classes. Size
50
classes included first feeding larvae, larvae of 20 to 30 mm, and 30 to 45 mm.
Experiments with first feeding larvae were initiated when the yolk sac was completely
absorbed, which was reported to be a more reliable criterion for the onset of exogenous
feeding in Acipenseridae compared to the evacuation of the melanin plug (Gisbert and
Williot 1997, Ghelichi et al. 2010, Rapp Chapter II). Thus, first feeding larvae were not
fed prior to the onset of the experiments, while other size classes were fed a mixed diet of
zooplankton and Chironomidae and Ephemeroptera larvae that were also used as prey
types in prey selection experiments.
Experiments were conducted in 38-L tanks equipped with aeration systems and
illumination. Tanks were filled with 30 L of dechlorinated tap water at a temperature of
17˚C. No filter system was used to avoid entrainment of larval pallid sturgeon and
zooplankton prey. Aeration was removed during prey selection trials and dissolved
oxygen and water temperature were assessed prior to trials using a handheld device
(Hach, Loveland, CO, USA, model: HQ40D multiparameter sonde). Due to the lack of
information on substrate preferences of larval pallid sturgeon and potential interactions of
prey accessibility and substrate type, no substrate was used. Prey accessibility may differ
between substrate types and also may vary between prey taxa (Ivlev 1961, Levin 1988).
For example, accessibility of pelagic zooplankton may not be influenced by substrate,
whereas accessibility of benthic invertebrates, such as Chironomidae larvae, is decreased
in larval pallid sturgeon due to burying and case building behavior of some
Chironomidae larvae (D. Deslaurier, personal communication, South Dakota State
51
University). The lack of substrate also ensured that the predetermined prey densities were
available to larval pallid sturgeon.
Prey selection was assessed for zooplankton and Chironomidae and
Ephemeroptera larvae. All three prey taxa were offered simultaneously in low and high
density combinations resulting in n = 8 treatments. Densities for zooplankton were based
on water volume and for Chironomidae and Ephemeroptera larvae were based on tank
bottom area. Low densities were 2.5 individuals/L for zooplankton and 25 individuals/m2
for Chironomidae and Ephemeroptera larvae. High densities were 25 individuals/L for
zooplankton and 500 individuals/m2 for Chironomidae and Ephemeroptera larvae. Low
and high prey densities were based on realistic densities for each taxa observed in the
Lewis and Clark Delta of the middle Missouri River during summer and early fall
(benthic invertebrates: Grohs 2008, zooplankton: Rapp Chapter IV). Zooplankton
densities were assessed for the two main taxa, Cladocera and Copepoda, but composition
differed between size classes. In trials with first feeding larvae zooplankton was
composed of 65.3 % Cladocera (primarily Daphnia spp.) and 34.6 % Copepoda, in trials
with fish from 20 to 30 mm was composed of 14.6 % Cladocera (primarily Daphnia spp.)
and 85.4 % Copepoda and in trials with fish from 30 to 45 mm was composed of 81.3 %
Cladocera (primarily Daphnia spp.) and 18.7 % Copepoda. Prey densities were
monitored and eaten prey was supplemented to avoid an influence of prey depletion on
prey selection. Due to the poor foraging ability of first feeding larvae and larvae of 20 to
30 mm, 10 individuals were simultaneously used during prey selection trials. A single
larva of 30 to 45 mm was used due to the improved foraging ability. Fish were starved for
52
12 h prior to the onset of the experiments. Fish were allowed to feed for 30 min and after
this time period larvae were euthanized and preserved in 10 % formalin solution for
stomach analysis. Pallid sturgeon larvae length, ingested prey taxa, and prey length were
recorded. Lengths were measured to the nearest 0.01 mm using a dissecting scope
(Olympus America, Mellville, NY, USA, model: SZH 10) with appropriate software
(Olympus America, Mellville, NY, USA, model: DP2-BSW, version: 2.2).
Prey selection of juvenile pallid sturgeon
Juvenile pallid sturgeon were obtained from the Gavins Point National Fish
Hatchery (Yankton, SD, USA) in 2010 and 2011. Fish were raised in a temperature-
controlled recirculating system at South Dakota State University at 20˚C, a day:night
light regime of 12:12 h, and were fed a commercially available pelleted food until they
approached the respective size classes for the prey selection experiments. Size classes
included 70 to 90 mm, 125 to 200 mm, 250 to 350 mm, and 351 to 450 mm fork length.
At least two weeks prior to the onset of the experiments, pallid sturgeon were switched to
a mixed diet of the prey types used in the prey selection experiments. Only fish from 70-
90 mm did not receive pelleted food and were fed a mixed diet of Chironomidae and
Ephemeroptera larvae from the start, which were the prey types used for prey selection
trials in this size class.
Experiments for juvenile pallid sturgeon ranging from 70-90 mm were conducted
in 38-L tanks. Fish ranging from 125 to 200 mm were tested in tanks with a volume of
53
250 L and fish ranging from 250 to 350 and 351 to 450 mm in tanks with a volume of
500 L. Tanks were equipped with aeration systems and illumination and were filled with
dechlorinated tap water maintained at 20˚C. Prior to the onset of the experiments aeration
was removed. Dissolved oxygen and water temperature were assessed at the beginning of
each trial using a handheld device (Hach, Loveland, CO, USA, model: HQ40D
multiparameter sonde). Juvenile pallid sturgeon show a strong preference for sand
substrate (Allen et al. 2007, Rapp unpublished data). Therefore each tank was supplied
with a 0.5 to 1 cm layer of sand.
Prey selection of juvenile pallid sturgeon from 70 to 90 mm, 125 to 200 mm was
assessed for Chironomidae and Ephemeroptera larvae. Prey selection of fish ranging from
250 to 350 and 351 to 450 mm was assessed for Chironomidae larvae and fish prey.
Separate trials were conducted with fathead minnows Pimephales promelas and Johnny
darters Etheostoma nigrum. Two prey types were offered simultaneously in low and high
density combinations resulting in n = 4 treatments. Densities for all prey types (i.e.,
Chironomidae and Ephemeroptera larvae and fish prey) were based on tank bottom area.
Low densities for Chironomidae and Ephemeroptera larvae were 50 individuals/m2 and
for fish prey was 5 individuals/m2. High densities for Chironomidae and Ephemeroptera
larvae were 250 individuals/m2 and for fish prey was 30 individuals/m2. Prey densities
were monitored and eaten prey was supplemented to avoid an influence of prey depletion
on prey selection. Pallid sturgeon were acclimated to the experimental tanks for 24 h
prior to the onset of the experiments and starved during the acclimation period. A single
54
pallid sturgeon was allowed to feed for 30 min. Pallid sturgeon were visually observed
and numbers eaten, attacks and successful captures were recorded for each prey type.
Statistical analyses
Prey selection patterns did not differ between fish ranging from 70 to 90 mm and
125 to 200 mm and fish were grouped into one size class of 70 to 200 mm. Similarly,
prey selection patterns were similar between fish ranging from 250 to 350 mm and 351 to
450 mm and fish were grouped into one size class of 250 to 450 mm. Individual first
feeding larvae and individual larvae of 20 to 30 mm were treated as sub-samples due to
the simultaneous use of 10 individuals. For other size classes fish were treated as
replicates. Fish that did not feed were excluded from analyses, which was particularly
observed in larval size classes and thus, the numbers of replicates differed between prey
density combinations. In first feeding larvae numbers of replicates ranged from 5 to 12, in
larvae from 20 to 30 mm numbers of replicates ranged from 8 to 16, and in larvae from
30 to 45 mm numbers of replicates ranged from 7 to 10. Prey selection experiments with
juvenile fish were replicated 5 times for each size class and prey density combination
(i.e., 10 replicates after re-grouping size classes in 70 to 200 mm and 250 to 450 mm).
Prey selection was analyzed using the χ2 - based V-Index (Pearre 1982) according
to the equation
55
where V represent the selectivity index value, ad represents taxon a in the diet and bd
represents all other taxa in the diet. The ae value represents availability of taxon a in the
environment and be represents all other taxa in the environment, and a represents ad + ae,
b represents bd + be, d represent ad + bd, and e represent ae + be. The V-index ranges from
-1 to 1 and a value of 0 indicates neutral selection. Prey selectivity was analyzed
separately for each replicate and selectivity values were pooled. Prey selection was
compared to neutral selection (i.e., 0) for each prey type with Wilcoxon one-sample
signed-rank tests and significance was assessed at α < 0.05. Significant differences from
neutral selection were judged as either positive or negative selection. Presented values are
means ± 95 % confidence intervals.
Graphical analysis was used to facilitate interpretation of feeding patterns and
prey importance by plotting prey-specific abundance (Pi) against frequency of occurrence
(Fi) (Costello 1990, Amundsen et al. 1996). The modified approach of Amundsen et al.
(1996) was used and prey-specific abundance was calculated according to
Pi = (∑ Si/ ∑Sti) × 100
where Pi represents the prey-specific abundance of prey i, Si is the number of prey i in the
stomach and Sti is the total number of stomach content in those predators that contain
prey i. Frequency of occurrence was calculated according to
56
Fi = (Ni/N) × 100
where Fi represents frequency of occurrence, Ni is the number of fish with prey i in the
stomach and N is the total number of fish with prey in the stomach.
Capture efficiency for each prey type within juvenile pallid sturgeon size classes
was compared using χ2 cross-table analysis and significance was judged at α < 0.05. The
χ2 cross-table analyses were conducted using the software package SPSS 21.0 (IBM,
Armonk, NY, USA).
RESULTS
Larval pallid sturgeon prey selection and food habits
Mean ± SD total length of first feeding larvae was 20.38 ± 2.18 mm. Pallid
sturgeon consumed all prey types and we observed neutral selection for both benthic
invertebrate taxa in 7 of the 8 density combinations and for zooplankton in 5 of the 8
density combinations (Figure 1). Graphical analysis revealed that Chironomidae larvae
were the dominant prey type in the diet when available in high densities at most prey
density combinations and frequently consumed by fewer fish when available in low
densities (Figure 2). Mean ± SD length of ingested Chironomidae larvae was 4.09 ± 1.94
mm. Similarly, Ephemeroptera larvae were the dominant prey types when available in
high densities and Chironomidae larvae were available in low densities, but were
infrequently consumed when available in low densities (Figure 2). Mean ± SD length of
57
ingested Ephemeroptera larvae (excluding tail filaments) was 2.39 ± 1.04 mm.
Zooplankton was the dominant prey type when both benthic invertebrate taxa were
available in low densities and was consumed by fewer fish in most other treatments
(Figure 2). Mean ± SD length of ingested zooplankton was 1.15 ± 0.55 mm, of which
Daphnia spp. comprised 100 % of the ingested taxa.
Mean ± SD total length of larvae in the 20 to 30 mm size class was 24.16 ± 1.90
mm. Pallid sturgeon consumed all prey types but selected positively for Chironomidae
larvae when available in high densities at most prey density combinations and neutrally
when available in low densities at most prey density combinations. Neutral selection for
Chironomidae larvae was mostly accompanied by higher or equal (either high or low
densities) availability of Ephemeroptera larvae (Figure 3). Mean ± SD length of ingested
Chironomidae larvae was 5.78 ± 1.35 mm. Ephemeroptera larvae were positively selected
when available in high densities and when Chironomidae larvae were simultaneously
available in low densities. When Ephemeroptera and Chironomidae larvae were equally
available, Ephemeroptera larvae were neutrally selected and when Ephemeroptera larvae
were available in lower densities than Chironomidae larvae, pallid sturgeon selected
either neutrally or negatively for Ephemeroptera larvae (Figure 3). Mean ± SD length of
ingested Ephemeroptera larvae (excluding tail filaments) was 2.72 ± 0.96 mm.
Zooplankton was negatively selected except when all prey types were available in low
densities at which zooplankton was neutrally selected (Figure 3). Mean ± SD length of
ingested zooplankton was 0.75 ± 0.64 mm, of which Daphnia spp. comprised 88.9 % of
the identifiable taxa in the pallid sturgeon diet. Similar to selection patterns, graphical
58
analysis revealed that Chironomidae larvae were the dominant prey type when available
in high densities in most treatments, whereas Ephemeroptera larvae were the dominant
prey type when available in high densities and Chironomidae larvae were simultaneously
available in low densities. Zooplankton was opportunistically consumed when available
in high densities and rarely when available in low densities. Only when both benthic prey
types were available in low densities zooplankton contributed considerably to the larval
pallid sturgeon diet (Figure 4).
Mean ± SD total length of larvae in the 30 to 45 mm size class was 34.81 ± 3.48
mm. Pallid sturgeon consumed all prey types but selected positively for Chironomidae
larvae when available in high densities in all but one treatment. Chironomidae were
neutrally selected when available in low densities and only when all other prey types
were also available in low densities Chironomidae larvae were positively selected (Figure
5). Mean ± SD length of ingested Chironomidae larvae was 5.05 ± 2.02 mm.
Ephemeroptera larvae were positively selected when available in high densities and
Chironomidae larvae were simultaneously available in low densities. In most other
treatments Ephemeroptera larvae were neutrally selected (Figure 5). Mean ± SD length of
Ephemeroptera larvae (excluding tail filaments) was 3.29 ± 1.89 mm. Zooplankton was
neutrally selected in 4 treatments and negatively selected in the other 4 treatments (Figure
5). Mean ± SD length of ingested zooplankton was 1.44 ± 0.47 mm, of which Daphnia
spp. comprised 100 % of the identifiable taxa in the pallid sturgeon diet. Graphical
analysis revealed that Chironomidae larvae were the dominant prey type in all but one
treatment when available in high densities. When Chironomidae were available in low
59
densities pallid sturgeon fed primarily on Ephemeroptera larvae and zooplankton.
Ephemeroptera larvae were rarely consumed when available in low densities.
Zooplankton was frequently consumed in most treatments and contributed considerably
to the pallid sturgeon diet when available in high densities (Figure 6).
Juvenile pallid sturgeon prey selection and food habits
Mean ± SD fork length of juvenile age-0 pallid sturgeon in the 70 to 200 mm size
class was 116.7 ± 42.3 mm. Age-0 pallid sturgeon selected positively for Chironomidae
larvae and negatively for Ephemeroptera larvae over most prey density combinations and
only when Chironomidae were available in high densities and Ephemeroptera larvae were
available in low densities neutral selection was observed (Figure 7). Graphical analysis
revealed that Chironomidae larvae were the dominant prey type over all density
combinations while Ephemeroptera larvae were rarely consumed when available in equal
or lower densities than Chironomidae larvae. Only when Ephemeroptera larvae were
available in high densities and Chironomidae larvae were simultaneously available in low
densities Ephemeroptera larvae contributed considerably to the pallid sturgeon diet
(Figure 8). Capture efficiency was significantly higher for Chironomidae larvae (78.5 %)
than for Ephemeroptera larvae (56.5 %) (χ2 = 21.892, df = 1, P < 0.01).
Mean ± SD fork length of juvenile pallid sturgeon in the 250 to 450 mm size class
was 352.2 ± 45.6 mm. Pallid sturgeon selected positively for Chironomidae larvae and
negatively for fish prey, either fathead minnows or Johnny darters (Figure 9, Figure 11).
60
Similarly, graphical analysis revealed that Chironomidae larvae were the dominant prey
type over all prey density combinations, while both types of fish prey were rarely
consumed. However, consumption of fish prey increased when Chironomidae larvae
were available in low densities and fish prey was available in high densities (Figure 10,
Figure 12). Neutral selection was observed when comparing both types of fish prey over
all density combinations (Figure 13). Graphical analysis revealed a similar pattern. When
fathead minnows and Johnny darters were available in equal densities both types of fish
prey were consumed in similar quantities. When available in unequal densities, the more
abundant prey fish species contributed more to the pallid sturgeon diet (Figure 14).
Capture efficiency differed significantly between prey types and was higher for
Chironomidae larvae (99.9 %) than for fathead minnows (41.1 %) and Johnny darters
(25.8 %) (χ2 = 2997.804, df = 2, P < 0.01).
DISCUSSION
Larval pallid sturgeon prey selection and food habits
First feeding pallid sturgeon larvae selected neutrally for Chironomidae and
Ephemeroptera larvae at most prey density combinations. However graphical analysis
revealed similar patterns to those observed in larger larvae ranging from 20 to 30 mm and
30 to 45 mm for which Chironomidae larvae were amongst the dominant prey types when
available in high densities, while Ephemeroptera were amongst the dominant prey types
when available in high densities and Chironomidae larvae were available in low
61
densities. In both larger size classes of 20 to 30 mm and 30 to 45 mm this pattern was
similar to prey selection patterns at which positive selection was observed for
Chironomidae larvae when available in high densities at most prey density combinations,
while positive selection for Ephemeroptera was only observed when available in high
densities and Chironomidae larvae were available in low densities. When available in
similar densities as Chironomidae larvae, Ephemeroptera larvae were mostly neutrally
selected. The observed selection and feeding patterns indicate a ranking of benthic prey
types in larval pallid sturgeon at which Chironomidae larvae are selected over
Ephemeroptera larvae, which may at least partially be caused by capture efficiency.
Although not assessed for larval fish, we showed that in age-0 pallid sturgeon capture
efficiency was higher for sluggish Chironomidae larvae (78.5 %) than for agile
Ephemeroptera larvae (56.5 %). Thus, it seems to be likely that the same applies to larvae
which are generally more restricted in prey capture and ingestion than juvenile fish
(Hunter 1981, Balon 1986, Houde 1987). In field studies, Chironomidae larvae and pupae
and Ephemeroptera larvae were frequently observed as the main prey items of small age-
0 pallid sturgeon (Braaten et al. 2012), Scaphirhynchus spp. (Sechler et al. 2012, 2013)
and shovelnose sturgeon (Braaten et al. 2007), while other prey types were rare or absent.
Zooplankton was neutrally or negatively selected in first feeding larvae, larvae of 20 to
30 mm and 30 to 45 mm. However graphical analysis revealed that zooplankton was
frequently consumed. Negative selection was caused by considerably higher densities of
zooplankton used in prey selection trials compared Chironomidae and Ephemeroptera
larvae, as it is frequently observed in natural environments, which represents a common
issue for interpretation of selectivity indices (Strauss 1979). As such graphical analysis is
62
likely more informative when comparing prey types that differ drastically in densities.
Zooplankton was amongst the dominant prey types at several prey density combinations
in first feeding larvae and larvae ranging from 30 to 45 mm, particularly when available
in high densities or when benthic prey was only available in low densities, however was
less consumed in fish ranging from 20 to 30 mm. The greater consumption of
zooplankton in larger (i.e., 30 to 45 mm) compared to smaller fish (i.e., 20 to 30 mm) is
counterintuitive and disagrees with previous studies on other Acipenseridae. For
example, Amirkolaie (2009) observed a decrease in zooplankton consumption and
increase in Chironomidae larvae consumption during ontogeny in Persian sturgeon
Acipenser persicus and Buckley and Kynard (1981) observed a switch from zooplankton
to benthic prey during the first weeks of exogenous feeding in shortnose sturgeon A.
brevirostrum. Collectively, these studies suggest a decreasing importance of zooplankton
and increasing importance of benthic prey in Acipenseridae, and as such an opposite
pattern to that observed in this study. Differences in zooplankton consumption may be
related to zooplankton composition, which differed between size classes. In prey
selection trials with fish ranging from 20 to 30 mm, zooplankton in the environment was
composed of 14.6 % Cladocera (particularly Daphnia spp.) and 85.4 % Copepoda, while
in trials with first feeding larvae was composed of 65.3 % Cladocera (particularly
Daphnia spp.) and 34.6 % Copepoda and in trials with larvae ranging from 30 to 45 mm
was composed of 81.3 % Cladocera (particularly Daphnia spp.) and 18.7 % Copepoda.
Ingested zooplankton was, however, for all size classes primarily composed of Daphnia
spp. (first feeding larvae: 100 %, 20 to 30 mm: 88.9 %, 30 to 45 mm: 100 %) and thus,
higher incorporation of zooplankton in first feeding larvae and larvae ranging from 30 to
63
45 mm may have been caused by greater availability of Daphnia spp. as prey.
Furthermore mean sizes of Daphnia spp. differed and individuals were larger in trials
with first feeding larvae and larvae ranging from 30 to 45 mm compared to those in trials
with fish in the 20 to 30 mm size class. Differences in consumption suggest that not all
zooplankton taxa represent appropriate prey for larval pallid sturgeon and particularly
Daphnia spp. are selected. Similarly, Amirkolaie (2009) observed primarily Daphnia spp.
in the diet of Persian sturgeon, which were selected over Copepoda. It was suggested for
other species that a decrease in large Daphnia spp. provoke a shift towards benthic
invertebrates (Mills and Forney 1981), which is similar to the observed trend in the
present study for fish ranging from 20 to 30 mm. Field studies generally did not report
zooplankton in the diet of small age-0 pallid sturgeon (Braaten et al. 2012),
Scaphirhynchus spp. (Sechler et al. 2012, 2013) or shovelnose sturgeon (Braaten et al.
2007). The complete lack of zooplankton in field samples of pallid and shovelnose
sturgeon may be related to differential digestion rate of prey items, which can bias field
samples (Gannon 1976, Strauss 1979). For example, Gannon (1976) observed rapid
digestion of Daphnia spp. compared to other zooplankton species or benthic
invertebrates, which resulted in underestimation of their importance as prey for alewife
Alosa pseudoharengus. An alternative explanation may be related to sampling locations
or river conditions, which can alter prey composition in field samples (Sechler et al.
2013). Daphnia spp. are often found in lentic inshore habitats including floodplains,
which have been severely reduced during impoundment and channelization of the
Missouri and Mississippi rivers. Fisher (2011) reported low Daphnia spp. densities (≤ 1.1
individuals/L) for main channel habitats in the upper Missouri River, but observed high
64
densities in backwater habitats and Rapp (Chapter IV) observed up to 37.8 Daphnia
spp./L in backwater habitats in the Lewis and Clark Delta of the middle Missouri River,
while densities in delta main and side channel habitats were generally less than 1.5
individuals/L. Similarly, high zooplankton densities were reported for created backwaters
and floodplains in the lower Missouri River, which exceeded those in other habitats
(Dzialowski et al. 2013, Gosch et al. 2014). Thus, low Daphnia spp. densities in Missouri
River main and side channel habitats may contribute to the lack of Daphnia spp. in age-0
pallid sturgeon field diet samples.
Collectively, our results indicate that Chironomidae larvae are the selected prey
type by larval pallid sturgeon, but other prey types are consumed when Chironomidae
larvae are rare. Furthermore, our results suggest that Daphnia spp. can contribute to the
diet of larval pallid sturgeon, while other zooplankton taxa are rarely consumed.
Juvenile pallid sturgeon prey selection and food habits
Juvenile pallid sturgeon ranging from 70 to 200 mm selected positively for
Chironomidae larvae and negatively for Ephemeroptera larvae in all but one treatment for
which neutral selection was observed. Graphical analysis revealed that Chironomidae
larvae are the dominant prey item, but importance of Ephemeroptera larvae increased
when available in high densities and Chironomidae larvae were available in low
densities. Chironomidae and Ephemeroptera larvae were reported to be the major prey
items of age-0 pallid sturgeon (Braaten et al. 2012), Scaphirhynchus spp. (Sechler et al.
65
2012, 2013, Harrison et al. 2014) and shovelnose sturgeon (Braaten et al. 2007). Braaten
et al. (2012) reported a great increase of Chironomidae larvae in the diet of pallid
sturgeon of 77 and 97 mm compared smaller individuals ranging from 48 to 56 mm,
while numbers of Ephemeroptera larvae were similar between sizes and lower than
Chironomidae larvae numbers. Selection of Chironomidae over Ephemeroptera larvae in
the present study was partially caused by higher capture efficiency of Chironomidae
larvae (78.5 %) compared to Ephemeroptera larvae (56.5 %). However, capture
efficiency does not fully explain differences in prey selection and feeding patterns as also
overall capture attempts were about 4 times higher for Chironomidae larvae than for
Ephemeroptera larvae. Similarly, Soriguer et al. (2002) reported higher capture efficiency
for sluggish prey, such as Tubificidae or Lumbricidae compared to agile prey including
Ephemeroptera larvae in Adriatic sturgeon A. naccarii and overall more capture attempts
for worm-type prey.
Juvenile pallid sturgeon ranging from 250 to 450 mm selected positively for
Chironomidae larvae and negatively for fish prey and graphical analysis revealed that
both types of fish prey were rarely consumed over all prey density combinations.
However, incorporation of fish prey increased when available in high densities and
Chironomidae larvae were only available in low densities. Importance of Chironomidae
larvae and other benthic invertebrates as forage for age-1 and age-2 pallid sturgeon has
been reported from field studies and although fish prey was incorporated in the diet of
juvenile pallid sturgeon of similar size and age, benthic invertebrates remained an
integral diet component also for larger fish (Wanner et al. 2007, Grohs et al. 2009).
66
Ingested fish prey of various sizes differed between field studies and frequently observed
taxa included Cyprinidae such as sturgeon chub Macrhybopsis gelida and sicklefin chub
Macrhybopsis meeki in the upper Missouri River above Fort Peck Reservoir (Gerrity et
al. 2006), Johnny darter in the middle Missouri River between Fort Randall Dam and
Lewis and Clark Lake (Grohs et al. 2009) and Cyprinidae, Sciaenidae, and Clupeidae in
the lower Missouri and Mississippi River (Carlson et al. 1985, Hoover et al. 2007). We
used fathead minnow, a ubiquitous cyprinid species, and Johnny darter, the main fish
prey in the Fort Randall Reach. Chironomidae larvae were positively selected
irrespective of prey fish species. Likewise, when comparing fathead minnow and Johnny
darter, we observed neutral selection for both fish species over all prey density
combinations. Graphical analysis revealed that when available in equal densities both
types of fish prey were similarly consumed and when available in unequal densities, more
frequent fish prey was consumed in higher numbers. Capture efficiency for both types of
fish prey was low (fathead minnow: 41.1 %, Johnny darter: 25.8 %) and similarly may
contribute to, but not fully explain, selection patterns, as also feeding attempts on fish
prey were less than 1 % of all attempts in Chironomidae larvae-fish prey trials. Based on
the observed feeding patterns and the lack of specialized adaptations for a piscivorous life
style, which may contribute to poor capture efficiency of fish prey, pallid sturgeon can be
categorized as secondary or opportunistic piscivore and incorporation of fish in the diet is
likely a result of fortuitous encounter or a gradual switch to larger prey in order to
maintain energetic efficiency (Keast 1985).
67
ACKNOWLEDGEMENTS
Funding for this study was provided by the US Army Corps of Engineers. We
thank the hatchery personnel at Gavins Point National Fish Hatchery for providing pallid
sturgeon. Laboratory assistance was provided by Jason Augspurger, Blake Bartz, Aaron
Burgad, Kevin Peery, and Tyler Trimpe.
68
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77
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Figure 3-1: Prey selection (V-index and 95 % confidence intervals) by first feeding
pallid sturgeon at 8 density combinations of Chironomidae larvae, zooplankton, and
Ephemeroptera larvae. Prey densities are either high or low and are indicated on top for
individual prey types. Positive selection is indicated by +, neutral selection is indicated
by ±, and negative selection is indicated by –.
78
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Figure 3-2: Food habits of first feeding pallid sturgeon. Prey-specific abundance (%) of
Chironomidae larvae, zooplankton and Ephemeroptera larvae is plotted against frequency
of occurrence (%) of each prey type. Diagonal axis from the lower left corner (rare prey
item) to the upper right corner (dominant prey item) indicates prey importance, vertical
axis indicates feeding strategy in terms of generalization (lower part of the graph) and
specialization (upper part of the graph). Plots located in the upper left corner indicate
high consumption of prey types by few individuals and plots in the lower right corner
indicate occasional consumption by many individuals.
79
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Figure 3-3: Prey selection (V-index and 95 % confidence intervals) by pallid sturgeon
ranging from 20 to 30 mm at 8 density combinations of Chironomidae larvae,
zooplankton, and Ephemeroptera larvae. Prey densities are either high or low and are
indicated on top for individual prey types. Positive selection is indicated by +, neutral
selection is indicated by ±, and negative selection is indicated by –.
80
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Frequency of occurence (%)0 20 40 60 80 100
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Figure 3-4: Food habits of pallid sturgeon ranging from 20 to 30 mm. Prey-specific
abundance (%) of Chironomidae larvae, zooplankton, and Ephemeroptera larvae is
plotted against frequency of occurrence (%) of each prey type. Diagonal axis from the
lower left corner (rare prey item) to the upper right corner (dominant prey item) indicates
prey importance, vertical axis indicates feeding strategy in terms of generalization (lower
part of the graph) and specialization (upper part of the graph). Plots located in the upper
left corner indicate high consumption of prey types by few individuals and plots in the
lower right corner indicate occasional consumption by many individuals.
81
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Figure 3-5: Prey selection (V-index and 95 % confidence intervals) by pallid sturgeon
ranging from 30 to 45 mm at 8 density combinations of Chironomidae larvae,
zooplankton, and Ephemeroptera larvae. Prey densities are either high or low and are
indicated on top for individual prey types. Positive selection is indicated by +, neutral
selection is indicated by ±, and negative selection is indicated by –.
82
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0 20 40 60 80 100
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Figure 3-6: Food habits of pallid sturgeon ranging from 30 to 45 mm. Prey-specific
abundance (%) of Chironomidae larvae, zooplankton, and Ephemeroptera larvae is
plotted against frequency of occurrence (%) of each prey type. Diagonal axis from the
lower left corner (rare prey item) to the upper right corner (dominant prey item) indicates
prey importance, vertical axis indicates feeding strategy in terms of generalization (lower
part of the graph) and specialization (upper part of the graph). Plots located in the upper
left corner indicate high consumption of prey types by few individuals and plots in the
lower right corner indicate occasional consumption by many individuals.
83
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Figure 3-7: Prey selection (V-index and 95 % confidence intervals) by pallid sturgeon
ranging from 70 to 200 mm at 4 different density combinations of Chironomidae and
Ephemeroptera larvae. Prey densities are either high or low and are indicated on top for
individual prey types. Positive selection is indicated by +, neutral selection is indicated
by ±, and negative selection is indicated by –.
84
Pre
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Figure 3-8: Food habits of pallid sturgeon ranging from 70 to 200 mm. Prey-specific
abundance (%) of Chironomidae and Ephemeroptera larvae is plotted against frequency
of occurrence (%) of each prey type. Diagonal axis from the lower left corner (rare prey
item) to the upper right corner (dominant prey item) indicates prey importance, vertical
axis indicates feeding strategy in terms of generalization (lower part of the graph) and
specialization (upper part of the graph). Plots located in the upper left corner indicate
high consumption of prey types by few individuals and plots in the lower right corner
indicate occasional consumption by many individuals.
85
-0,6
-0,4
-0,2
0,0
0,2
0,4
0,6 High High
-0,6
-0,4
-0,2
0,0
0,2
0,4
0,6
Prey types
High Low
-0,6
-0,4
-0,2
0,0
0,2
0,4
0,6
Chironomidae Fathead minnow
Prey type
Low High
V-I
nd
ex
-0,6
-0,4
-0,2
0,0
0,2
0,4
0,6
Chironomidae Fathead minnow
Low Low
+_
+_
+_
+_
Figure 3-9: Prey selection (V-index and 95 % confidence intervals) by pallid sturgeon
ranging from 250 to 450 mm at 4 different density combinations of Chironomidae larvae
and fathead minnow. Prey densities are either high or low and are indicated on top for
individual prey types. Positive selection is indicated by + and negative selection is
indicated by –.
86
Pre
y-s
pec
ific
ab
un
dan
ce (
%)
0
20
40
60
80
100
Chironomidae: high
Minnow: high
0
20
40
60
80
100
Chironomidae: high
Minnow: low
0 20 40 60 80 100
0
20
40
60
80
100
Chironomidae: low
Minnow: high
Frequency of occurence (%)
0 20 40 60 80 100
0
20
40
60
80
100
Chironomidae: low
Minnow: low
Figure 3-10: Food habits of pallid sturgeon ranging from 250 to 450 mm. Prey-specific
abundance (%) of Chironomidae larvae and fathead minnow is plotted against frequency
of occurrence (%) of each prey type. Diagonal axis from the lower left corner (rare prey
item) to the upper right corner (dominant prey item) indicates prey importance, vertical
axis indicates feeding strategy in terms of generalization (lower part of the graph) and
specialization (upper part of the graph). Plots located in the upper left corner indicate
high consumption of prey types by few individuals and plots in the lower right corner
indicate occasional consumption by many individuals.
87
-0,6
-0,4
-0,2
0,0
0,2
0,4
0,6 High High
-0,6
-0,4
-0,2
0,0
0,2
0,4
0,6
Prey types
High Low
-0,6
-0,4
-0,2
0,0
0,2
0,4
0,6
Chironomidae Johnny darter
Prey type
Low High
V-I
nd
ex
-0,6
-0,4
-0,2
0,0
0,2
0,4
0,6
Chironomidae Johnny darter
Low Low
+_
+_ +
_
+_
Figure 3-11: Prey selection (V-index and 95 % confidence intervals) by pallid sturgeon
ranging from 250 to 450 mm at 4 different density combinations of Chironomidae larvae
and Johnny darter. Prey densities are either high or low and are indicated on top for
individual prey types. Positive selection is indicated by + and negative selection is
indicated by –.
88
Pre
y-s
pec
ific
ab
un
dan
ce (
%)
0
20
40
60
80
100
Chironomidae: high
Johnny darter: high
0
20
40
60
80
100
Chironomidae: high
Johnny darter: low
0 20 40 60 80 100
0
20
40
60
80
100
Chironomidae: low
Johnny darter: high
Frequency of occurence (%)
0 20 40 60 80 100
0
20
40
60
80
100
Chironomidae: low
Johnny darter: low
Figure 3-12: Food habits of pallid sturgeon ranging from 250 to 450 mm. Prey-specific
abundance (%) of Chironomidae larvae and Johnny darter is plotted against frequency of
occurrence (%) of each prey type. Diagonal axis from the lower left corner (rare prey
item) to the upper right corner (dominant prey item) indicates prey importance, vertical
axis indicates feeding strategy in terms of generalization (lower part of the graph) and
specialization (upper part of the graph). Plots located in the upper left corner indicate
high consumption of prey types by few individuals and plots in the lower right corner
indicate occasional consumption by many individuals.
89
-0,6
-0,4
-0,2
0,0
0,2
0,4
0,6 High High
-0,6
-0,4
-0,2
0,0
0,2
0,4
0,6
Prey types
High Low
-0,6
-0,4
-0,2
0,0
0,2
0,4
0,6
Fathead minnow Johnny darter
Prey type
Low High
V-I
nd
ex
-0,6
-0,4
-0,2
0,0
0,2
0,4
0,6
Fathead minnow Johnny darter
Low Low
± ±
± ±
± ±
± ±
Figure 3-13: Prey selection (V-index and 95 % confidence intervals) by pallid sturgeon
ranging from 250 to 450 mm at 4 different density combinations of fathead minnow and
Johnny darter. Prey densities are either high or low and are indicated on top for individual
prey types. Both types of fish prey were neutrally selected as indicated by ±.
90
Pre
y-s
pec
ific
ab
un
dan
ce (
%)
0
20
40
60
80
100
Minnow: high
Johnny darter: high
0
20
40
60
80
100
Minnow: high
Johnny darter: low
0 20 40 60 80 100
0
20
40
60
80
100
Minnow: low
Johnny darter: high
Frequency of occurence (%)
0 20 40 60 80 100
0
20
40
60
80
100
Minnow: low
Johnny darter: low
Figure 3-14: Food habits of pallid sturgeon ranging from 250 to 450 mm. Prey-specific
abundance (%) of fathead minnow and Johnny darter is plotted against frequency of
occurrence (%) of each prey type. Diagonal axis from the lower left corner (rare prey
item) to the upper right corner (dominant prey item) indicates prey importance, vertical
axis indicates feeding strategy in terms of generalization (lower part of the graph) and
specialization (upper part of the graph). Plots located in the upper left corner indicate
high consumption of prey types by few individuals and plots in the lower right corner
indicate occasional consumption by many individuals.
91
CHAPTER IV
SHALLOW WATER HABITAT EVALUATION IN THE LEWIS AND CLARK
DELTA, WITH A FOCUS ON NURSERY HABITAT SUITABILITY FOR PALLID
STURGEON
ABSTRACT
Shallow water habitats are important components of large river ecosystems and
serve as nurseries for many fishes, but have been degraded in many systems due to river
modifications. The loss of shallow water habitats in the Missouri River was identified as
potential cause for recruitment failure of pallid sturgeon Scaphirhynchus albus.
Consequently, recovery effort has focused on habitat restoration, however, nursery
habitat requirements for pallid sturgeon are largely unknown. We conducted a study in
the Lewis and Clark Delta of the Missouri River to evaluate four shallow water habitat
types regarding their suitability as nurseries for pallid sturgeon. Habitat types included
backwaters, side channels, main channel depositional zones, and Lewis and Clark Lake
headwater habitats. We used a mesocosm approach and compared growth, energy density
and survival of pallid sturgeon among habitat types and included a laboratory reference
baseline in the assessment. In addition, physical habitat characteristics, water quality
variables, nutrient concentrations, algal biomass (i.e. chlorophyll α concentrations),
macrophyte density, and zooplankton and benthic invertebrate densities were assessed to
identify variables that foster growth and condition (i.e. energy density) of pallid sturgeon.
92
Chlorophyll a concentration and macrophyte density were higher in backwaters
compared to main channel and Lewis and Clark Lake headwater habitats, respectively.
Furthermore, higher zooplankton densities were observed in backwaters for several taxa,
particularly Daphnia spp., compared to other habitat types. Densities of most benthic
invertebrate taxa did not differ significantly among habitat types. However, total benthic
invertebrate density of taxa that constitute common prey for pallid sturgeon differed
among habitat types and tended to be highest in backwater habitats. Pallid sturgeon
growth, energy density, and survival did not differ among habitat types or the laboratory
reference baseline. However, high variability in pallid sturgeon growth and energy
density was observed within habitat types and we clustered sites that fostered high and
low growth and high and low energy density. While variables did not differ significantly
between sites that fostered high and low growth, sites that fostered high pallid sturgeon
energy density had lower velocities, smaller mean sediment grain size, higher
macrophyte density, and higher zooplankton and benthic invertebrate densities than sites
that caused low energy density. Regression analysis revealed that pallid sturgeon energy
density increased with increasing Ephemeridae and Caenidae larvae densities.
Ephemeridae larvae density was positively correlated with chlorophyll α concentration
and proportion of clay and silt in the river sediment and Caenidae larvae density was
negatively correlated with velocity and was positively correlated with macrophyte
density. Overall, the results suggest that conservation and rehabilitation of low velocity
habitats with fine substrate suitable for macrophyte colonization and enhanced algal
production, which foster benthic invertebrate colonization, may ultimately benefit age-0
pallid sturgeon.
93
INTRODUCTION
During the past centuries many rivers have been regulated through damming,
diversion, and channelization to meet water and energy demands, mitigate flood
consequences and facilitate navigation (Ward and Stanford 1989, Benke 1990).
Fragmentation and channelization alter the river’s flow regime, which is considered a key
variable, with subsequent effects on geomorphology, water quality (e.g., water
temperature), habitat structure, and ecological functions, collectively threatening the
integrity of riverine ecosystems (Karr 1991, Poff et al. 1997). Many of these
consequences were also reported for the Missouri River, which was extensively modified
and is one of the most regulated rivers within the United States (Hesse et al. 1989, Galat
et al. 2005). Consequently, it was recognized as North America’s most endangered river
in 1997, 2001, and 2002 by the organization American Rivers (American Rivers 1997,
2001, 2002).
Historically, the Missouri River was a mosaic of braided, shifting channels with
wide floodplains (Hesse et al. 1989, Galat et al. 2005). Erosion caused high sediment
loads and sediment deposition formed diverse habitats, such as pools, sandbars, islands,
side channels, and backwaters with substantial amounts of woody debris from eroded
riparian and island habitats (Hesse et al. 1989, Galat et al. 1998). The hydrograph was
characterized by two spring pulses in March and in June caused by snow melt and run-off
from the Great Plains and the Rocky Mountains, respectively, and declining flow from
summer through winter (Hesse et al. 1989, Galat et al. 1998, 2005).
94
During the 20th century the upper and middle Missouri River was impounded by
construction of six dams from Fort Peck Dam, Montana to Gavins Point Dam, South
Dakota (Hesse et al. 1989, Galat et al. 1996, 2005). Longitudinal fragmentation and
emergence of lentic sections pose a major interruption on the river flow and peak flows
during spring are less pronounced and base flow from summer through winter has
increased (Hesse et al. 1989, Galat et al. 1998, 2005). The altered hydrograph and
impoundment reduced erosion and channel migration, trapped sediment in main-stem
reservoirs, which collectively decreased annual suspended sediment load by 67 to 99 %
in the lower Missouri River (Galat et al. 1996). The water temperature decreased due to
hypolimnetic water release from dams (Galat et al. 2005), which also depresses
temperatures in downstream reaches (Ward and Stanford 1983). The lower Missouri
River was channelized from Sioux City, Iowa to St. Louis, Missouri to facilitate
navigation, which transformed the historically wide offset V-shaped channel with
variable depth and flows into a narrow U-shaped channel with uniform depth and high
flow rates (Hesse and Sheets 1993). Levees disconnect the river from its floodplains
(Galat et al. 1996, 2005), which are highly productive zones in riverine ecosystems (Junk
et al. 1989, Sparks 1995). Today, the inundated area is reduced by 90 % during the
average flood pulse relative to historic conditions (Hesse et al. 1989) and Hesse and
Sheets (1993) questioned that autotroph productivity can compensate for the reduced
energy influx from floodplains. Snag removal and deforestation, which already
commenced during the 19th century to facilitate steamboat navigation, considerably
decreased woody debris (Hesse and Sheets 1993, Galat et al. 2005), which supports high
densities of aquatic invertebrates (Benke et al. 1985, Galat et al. 2005) and provides
95
refuge for fish (Crook and Robertson 1999). Collectively, damming and channel
modifications altered the flow and temperature regimes, reduced habitat heterogeneity,
and resulted in a substantial loss of historically prevalent shallow water habitats (Hesse
and Sheets 1993, Galat et al. 1996, Bowen et al. 2003).
Shallow water habitats including backwaters, side channels and depositional
zones are important components of large river ecosystems. They are characterized by
lower velocities and increased water retention time compared to main channel habitats
(Bowen et al. 2003, Schiemer et al. 2001) stimulating algae and macrophyte growth
(Thorp 1992, Ward and Stanford 1995), which are often rare or absent from main
channels due to high velocities, limited light penetration, and unstable substrate (Peltier
and Welch 1969, Chambers et al. 1991, Madsen et al. 2001). Furthermore, the importance
of shallow water habitats for secondary production has been reported. Several studies
observed higher zooplankton densities, particularly in backwaters, which was attributed
to longer water retention time, low velocities, less turbulence, and lower turbidity
(Vranovský 1995, Schiemer et al. 2001, Burdis and Hoxmeier 2011, Fisher 2011,
Dzialowski et al. 2013). Vranovský (1995) documented zooplankton drift out of side
channels at velocities as low as 1 cm/s and Schiemer et al. (2001) concluded that most
zooplankton present in the main channel are produced in inshore habitats in large river
ecosystems and, thus, inshore habitats may substantially contribute to main channel
zooplankton densities. In addition, the significance of shallow water habitats for benthic
invertebrates has been addressed. Shallow water habitats are generally more
heterogeneous than main channel habitats and lower velocities and longer water retention
96
time facilitate accumulation of organic matter and drift wood and stimulate primary
productivity, which collectively provides favorable conditions for benthic invertebrate
colonization (Thorp 1992, Thorp and Delong 1994, Ward and Stanford 1995). Low
velocities, longer water retention time, habitat heterogeneity and increased primary and
secondary productivity can also benefit riverine fishes. Schiemer et al. (2001)
emphasized the importance of low velocities and longer water retention time for larval
fish, which are subjected to poor swimming ability, and highlighted the importance of
diverse microhabitat availability during the succession of the early ontogeny. In addition,
it was shown that the temperature regime in shallow water habitats is decoupled from
main channel habitats and higher water temperatures during summer can provide
favorable conditions for larval and juvenile fish growth (Schiemer et al. 2001, 2002)
during the critical period when early life stages are particularly sensitive to size and
growth selective mortality (Houde 1987, Miller et al. 1988, Sogard 1997, Takasuka et al.
2003). Structure (e.g., drift wood or macrophytes) provides shelter and decreases
predation (Crooke and Robertson 1999). Increased secondary production provides
important prey resources benefiting a variety of riverine fish species, at which the
significance of shallow water habitats particularly as nurseries has been emphasized
(Schiemer et al. 2001, 2002). Previous work suggests that suitable nursery habitats in
regulated rivers are rare in absence of retention zones (Schiemer et al. 2001), which is
hypothesized to contribute to the decline of several native riverine fishes in the Missouri
River. One of these species is the pallid sturgeon Scaphirhynchus albus, which was listed
as federally endangered under the Endangered Species Act in 1990, due to consistent
recruitment failure or insufficient recruitment throughout its range (Dryer and Sandvol
97
1993). Consequently, recovery effort has focused on shallow water habitat restoration
however nursery habitat requirements for pallid sturgeon are largely unknown.
To inform habitat restoration efforts we conducted a field study in the Lewis and
Clark Delta of the middle Missouri River to assess four shallow water habitat types
regarding their suitability as nurseries for pallid sturgeon. Habitat types included
backwaters, side channels, main channel depositional zones, and headwater habitats in
Lewis and Clark Lake. We used a mesocosm approach to compare growth, energy
density and survival of pallid sturgeon among habitat types and included a laboratory
reference baseline in the assessment. In addition, physical habitat characteristics, water
quality variables, nutrient concentrations, chlorophyll α concentration, macrophyte
density, and zooplankton and benthic invertebrate densities were assessed to identify
variables that foster growth and condition of pallid sturgeon.
METHODS
Study site
The study was conducted in the Fort Randall Reach of the Missouri River, which
is located between Fort Randall Dam and Gavins Point Dam. Fort Randall Reach is
characterized by an upper riverine section, a delta formed by sedimentation from the
Niobrara River (hereafter referred to as Lewis and Clark Delta), and Lewis and Clark
Lake, the lowermost of the six main-stem reservoirs. The lower portion of Fort Randall
98
Reach, which includes the Lewis and Clark Delta, was selected in the Pallid Sturgeon
Recovery Plan as part of the Research Priority Management Area 3, based on habitat
suitability for restoration and recovery of pallid sturgeon (Dryer and Sandoval 1993). The
Lewis and Clark Delta extends from the Niobrara River confluence to the headwaters of
Lewis and Clark Lake, features two main channels, and resembles many morphological
characteristics of the historic Missouri River, such as backwaters and side channels. All
study sites were located at the downstream end of the Lewis and Clark Delta between the
city of Springfield and the headwaters of Lewis and Clark Lake (Figure 1).
Experimental animals
Pallid sturgeon were obtained on September 3, 2013 from the Garrison Dam
National Fish Hatchery (Riverdale, ND, USA) and transported to South Dakota State
University, where they were held in a temperature-controlled laboratory. From a larger
pool of fish, one hundred similar sized individuals were randomly selected and placed in
a separate holding tank [L × W × H (cm): 110.5 × 110.5 × 40.5]. Tanks were filled with
dechlorinated tap water and fish were kept at 20˚C and a day:night light regime of 12:12
h. Fish were fed frozen Chironomidae larvae (Meyer 2011). Partial water exchanges were
conducted daily and water parameters were monitored to ensure adequate water quality
according to the Upper Basin Pallid Sturgeon Propagation Plan (US Fish and Wildlife
Service 2005). Dissolved oxygen and water temperature were measured using a handheld
device (Hach, Loveland, CO, USA, model: HQ40D multiparameter sonde) and ammonia
99
and nitrite were measured spectrophotometrically (ammonia: Hach method 8038, nitrite:
Hach method 8507). Fish remained in the holding tanks until the start of the field
experiment.
Data collection
The field study was conducted from September 16 to September 25, 2013.
Mesocosms [L × W × H (cm): 63.5 × 50.8 × 38.1, mesh size: 0.32 cm] were deployed at
five backwater sites, five Lewis and Clark Lake headwater sites, five main channel
depositional zones (hereafter referred to as main channel sites), and five side channel
sites. On four sites of each habitat type three mesocosms were deployed and at each one
site two mesocosms were deployed (n = 56 mesocosms). Individual mesocosms were
treated as sub-samples. Study sites were selected based on water depth and velocity.
Target water depth was between 0.5 m and 1 m, owing to the focus of the pallid sturgeon
recovery program on shallow water habitat restoration, and target velocity was ≤ 15 cm/s
owing to the swimming performance of age-0 pallid sturgeon (Adams et al. 1999, 2003).
From the pool of sites that met these criteria, study sites were randomly selected.
Mesocosms were attached to the river bottom with metal stakes and individually marked.
At each site a temperature logger was deployed. Study sites were left undisturbed for a
minimum of one week prior to the start of the experiment to allow for invertebrate
recolonization. On September 16, one randomly chosen pallid sturgeon was placed in
each mesocosm after fork length measurement to the nearest mm (mean ± SD: 67.8 ± 2.3
100
mm). Mesocosms were controlled daily from the outside and debris was removed.
Habitat and water quality variables were measured concurrently with the field study and
included velocity, triplicate samples of water depth, dissolved oxygen, pH, salinity,
conductivity, duplicate samples of turbidity, and total dissolved solids. Macrophyte cover
and the occurrence of drift wood were recorded at each site and grouped in 5 categories
based on density (0 = 0 %, 1 = 1-25 %, 2 = 26-50 %, 3 = 51-75 %, 4 = 76-100 %). Drift
wood was not observed at any of the study sites and was dropped from further
assessment. Zooplankton and benthic invertebrate samples, water samples, and sediment
samples were collected at each site during the study period (see below for details). On
September 25, mesocosms were recovered and pallid sturgeon were euthanized and
measured for fork length to the nearest mm. Digestive tracts were removed and preserved
in 10 % formalin solution for diet analysis. Fish carcasses were frozen until calorimetric
analysis. To assess energy density, fish carcasses were freeze-dried to a constant weight,
homogenized, pressed into pellets, and combusted in a bomb calorimeter (Parr
Instruments, Moline, IL, USA, model: 6200).
Zooplankton and benthic invertebrate sampling
Zooplankton and benthic invertebrates were collected at each site. Zooplankton
samples were collected with a tube sampler (diameter: 7.5 cm) and were filtered through
a 63 µm mesh. Five sub-samples were collected per site and samples were preserved in
10 % formalin solution. Benthic invertebrates were collected using stovepipe samplers
101
and D-frame nets (Turner and Trexler 1997). The stovepipe sampler consisted of open
ended cylindrical pipe measuring 34 cm in diameter and a dip net (500 µm mesh). The
stovepipe sampler was used by forcing the pipe into the bottom substrate and the dip net
was swirled to capture invertebrates enclosed in the stovepipe. Retained material was
washed into a collection tray, filtered through a 500-μm sieve, washed into plastic
containers and preserved in 10 % formalin solution. Invertebrate collection with the D-
frame net [W × H (cm): 45.7 × 22.9, 500-μm] included one 1 m sweep above the
sediment. All retained material was washed into a collection tray and filtered through a
500-μm sieve. Filtered material was washed in plastic containers and preserved in 10 %
formalin solution. Five sub-samples were collected for stovepipe samplers and D-frame
nets per site.
Water and sediment analyses
Duplicate water samples were collected at each site for chlorophyll α, total
suspended solids, total volatile solids, total nitrogen, nitrate-N, nitrite-N, ammonia-N,
total phosphorus, total dissolved phosphorus, orthophosphate-P, and soluble silica
analyses. Samples for chlorophyll α analysis were filtered through a grade GF/F glass
microfiber filter (GE Healthcare, Whatman, Pittburgh, PA, USA) and 10 drops of
supersaturated magnesium carbonate solution was added to avoid acid-induced
degradation of chlorophyll α. Filters were placed in vials with 96 % ethanol solution,
boiled in a water bath at 78˚C and stored in a refrigerator for 24 h (Sartory and
102
Grobbelaar 1984). Chlorophyll a concentration was then determined fluorometrically
(Turner Designs, Sunnyvale, CA, model: TD-700). Water samples for analysis of total
suspended solids and total volatile solids were filtered through a pre-weighted grade 934-
AH glass microfiber filter (GE Healthcare, Whatman, Pittburgh, PA, USA). Filter paper
and retained material was dried at 105˚C to assess total suspended solids (USEPA 1979a)
and then ignited at 550˚C to assess total volatile solids (US Environmental Protection
Agency 1979b). Total volatile solids were calculated as the difference between total
suspended solids and total non-volatile solids (US Environmental Protection Agency
1979b). Water samples for total nitrogen and total phosphorus analyses were not treated,
while samples for nitrate-N, nitrite-N, ammonia-N, total dissolved phosphorus,
orthophosphate-P, and soluble silica analyses were filtered through a 0.45 µm cellulose
acetate filter (GE Healthcare, Whatman, Pittburgh, PA, USA). All samples were analyzed
spectrophotometrically (Hach, Loveland, CO, USA, model: DR 3900 and DRB 200) with
the respective reagents (total nitrogen: Hach method 10071, nitrate-N: Hach method
8171, nitrite-N: Hach method 8507, ammonia-N: Hach method 8038, total phosphorus:
Hach method 8190, total dissolved phosphorus: Hach method 8190, orthophosphate-P:
Hach method 8048, soluble silica: Hach method 8185).
Duplicate sediment surface samples were collected at each site using a core
sampler. Sediment was analyzed for grain size by wet and dry sieving (US Environmental
Protection Agency 2003). To assess total volatile solids, which served as proxy for
organic matter in the sediment, sediment was dried to a constant weight at 105˚C, ignited
at 550˚C, and weight loss was assessed (US Environmental Protection Agency 2003).
103
Initial condition and laboratory reference baseline
Concurrent with the field study, laboratory reference baselines were established.
At the day of the onset of the field experiment 10 of the 100 initially separated pallid
sturgeon were euthanized, measured for fork length, and digestive tracts were removed.
Fish carcasses were frozen for calorimetric analysis to assess the condition of the fish at
the start of the experiment. Another 10 fish were measured for fork length, individually
transferred into 38-L tanks and grown concurrently with the field experiment. Tanks were
filled with 30 L of dechlorinated tap water at a temperature of 20˚C similar to the
Missouri River water temperature. Holding tanks were equipped with aeration systems
and illumination at a day:night light regime of 12:12 h. Pallid sturgeon were fed
Chironomidae larvae at 950 individuals/m2 (Rapp Chapter II). Partial daily water
exchanges (10 L) were conducted to ensure adequate water quality and exclude an
influence of water deterioration on growth and survival. Dissolved oxygen and water
temperature were measured using a handheld device (Hach, Loveland, CO, USA, model:
HQ40D multiparameter sonde) and water ammonia and nitrite were measured
spectrophotometrically (ammonia: Hach method 8038, nitrite: Hach method 8507) to
maintain acceptable levels for pallid sturgeon according to the Upper Basin Pallid
Sturgeon Propagation Plan (US Fish and Wildlife Service 2005). On the day the field
experiment was terminated, the laboratory fish were euthanized and measured for fork
length. Digestive tracts were removed and fish carcasses were frozen until calorimetric
analysis as described before.
104
Statistical analyses
Continuous variables were compared among habitat types using one-way analysis
of variance (ANOVA) followed by Tukey post-hoc tests after verifying that data meet the
assumptions of parametric tests. Assumption of normality was tested with Shapiro-Wilk
tests and assumption of variance homogeneity was tested with Levene’s tests. If
underlying assumptions were violated, a logarithmic transformation [ln(x+1)] was
applied. Proportion data was arcsine square root transformed prior to their use in
statistical analyses. If the transformation did not result in normal distribution a non-
parametric Kruskal-Wallis-H tests was used and when transformations did not result in
variance homogeneity a Dunnett’s-D3 post-hoc test for heterogeneous variances was
applied.
To further explore pallid sturgeon growth and energy density a two-step cluster
analyses was used to regroup sites based on growth and energy density. For both
variables, a two cluster solution was identified. Habitat variables, water quality variables,
nutrient concentrations, chlorophyll α concentration, macrophyte density, and
zooplankton and benthic invertebrate densities were compared between the two clusters
(i.e., low and high growth and energy density, respectively) using t-tests after verifying
that assumptions for parametric tests are met. In case of violation of underlying
assumptions a logarithmic transformation was applied [ln(x+1)]. Proportion data was
arcsine square root transformed prior to their use in statistical analyses. If the
transformation did not result in normal distribution a non-parametric Mann-Whitney-U
105
test was used and in case the transformation did not result in variance homogeneity a t-
test with adjustments for heterogeneous variances was applied.
We evaluated predictor variable importance for chlorophyll α concentration,
macrophyte density, zooplankton and benthic invertebrate densities, and pallid sturgeon
growth and energy density. Habitat variables, water quality variables and nutrient
concentrations were included to assess their importance for chlorophyll α concentration
and macrophyte density. Habitat variables, water quality variables, chlorophyll α
concentration, and macrophyte density were used to identify their importance for
zooplankton and benthic invertebrate densities. Lastly, habitat variables, water quality
variables, chlorophyll α concentration, macrophyte density, and zooplankton and benthic
invertebrate densities were used to identify their importance for pallid sturgeon growth
and energy density. Variables that deviated from normality were transformed using Box-
Cox power transformations. To evaluate predictor variable importance we used zero-
order correlations to identify and exclude variables that were not significantly correlated
with the dependent variable followed by hierarchical partitioning to identify predictor
variables with significant independent contributions to explain the dependent variable
(Murray and Connor 2009). Predictor variables with significant independent
contributions were then used in multiple regression analyses to obtain a measure of
model fit. Significance for all analyses was judged at α < 0.1. Statistical analyses were
conducted using SPSS 21.0 (IBM, Armonk, NY, USA) except for Box-Cox power
transformations and hierarchical partitioning which were conducted in R 3.1.1 (R
Development Core Team 2014) using the AID package (Dag et al. 2014) and the hier.part
106
package (Walsh and Mac Nally 2014), respectively. All results are presented as non-
transformed values to facilitate interpretation.
RESULTS
Habitat
Headwater and main channel habitats were significantly shallower than side
channel habitats (Table 1). Velocity was significantly lower and mean sediment grain
size was significantly smaller at backwater and main channel habitats compared to
headwater habitats (Table 1). Sediment at backwater habitats was primarily composed of
very fine (grain size: 0.063 to 0.125 mm) and fine sand (grain size: 0.125 to 0.250 mm)
and at headwater habitats was composed of fine and medium sand (grain size: 0.250 to
0.5 mm). Sediment at three main channel sites was primarily composed of very fine and
fine sand and at two sites was composed of clay, silt (grain size: < 0.063 mm) and very
fine sand. Side channel habitats were the most heterogeneous and sediment was primarily
composed of very fine sand at 3 sites and fine sand and medium sand at each one site.
Total volatile solids, which served as indicator of organic matter, was significantly higher
at main channel habitats compared to headwater habitats (Table 1).
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Water quality
Mean water temperature differed between habitat types and tended to be lower at
backwater habitats compared other habitat types, however post-hoc tests did not reveal
significant differences at α < 0.1. Mean concentration of total volatile solids was
significantly higher at headwater habitats than side channel habitats, while all other water
quality variables did not differ significantly between habitat types (Table 2).
Nutrient concentrations
Mean total nitrogen concentrations did not differ between habitat types, however
significant differences were observed for concentrations of inorganic nitrogen
compounds. Mean nitrate-N concentration was significantly lower at backwater habitats
compared to headwater, main channel, and side channel habitats and mean nitrite-N
concentration was lower at headwater habitats compared to main channel and side
channel habitats (Table 3). No significant differences were observed for any of the
phosphorus variables (i.e., total phosphorus, total dissolved phosphorus, and
orthophosphate-P; Table 3). Mean soluble silica concentration was significantly higher at
backwater habitats compared to side channel habitats (Table 3).
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Chlorophyll α concentration and macrophyte density
Mean chlorophyll α concentration was significantly higher at backwater habitats
(mean ± SE: 26.52 ± 3.11 μg/L) compared to main channel habitats (mean ± SE: 17.88 ±
0.71 μg/L), while headwater habitats (mean ± SE: 22.59 ± 1.17 μg/L) and side channel
habitats (mean ± SE: 20.44 ± 2.50 μg/L) had intermediate chlorophyll α concentrations
(ANOVA, F = 3.004, df = 3, P = 0.06). Total phosphorus and nitrate-N concentrations
explained 44.7 % of the variation in chlorophyll a concentration (P = 0.01). Sites with
high chlorophyll α concentration had higher total phosphorus and lower nitrate-N
concentrations.
Macrophytes were present at all backwater habitats in variable densities
(categories 1 to 3; i.e., 1 to 75 %), while at the Lewis and Clark headwater habitats
macrophytes were only present at one site in low density (category 1; 1 to 25 %,).
Macrophytes were also present at 3 main channel sites in low densities (category 1; 1 to
25 %) and at 3 side channel sites in variable densities (categories 2 to 3; 26 to 75 %).
Differences in macrophyte density were significant between backwater habitats and
headwater habitats (Kruskal-Wallis-H, χ2 = 7.036, df = 3, P = 0.07). Variation in
macrophyte density was best explained by water depth and velocity (r2 = 0.79, P < 0.01)
at which macrophyte density increased with increasing water depth and decreasing
velocities.
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Zooplankton
Mean Rotifera density differed significantly between habitat types and tended to
be higher at backwater and headwater habitats compared to main channel and side
channel habitats, however post-hoc tests did not reveal significant results at α < 0.1
(Table 4). Mean Copepoda density did not differ significantly between habitat types
(Table 4). Daphnia spp. were the most frequently observed Cladocera taxa and mean
densities were significantly higher at backwater habitats compared to all other habitat
types (Table 4). Other Cladocera taxa (Bosmina spp., Chydorus spp., and Ceriodaphnia
spp.) only occurred in low densities and were analyzed together. Mean Cladocera density
was significantly higher at backwater habitats compared to side channel habitats and also
tended to be higher relative to headwater and main channel habitats (Table 4). Ostracoda
were only observed at 4 sites in low densities and were therefore not analyzed separately,
but included in the total zooplankton analysis. Mean total zooplankton density differed
significantly between habitat types and tended to be higher at backwater habitats,
however variability within habitat types was high and post-hoc test did not reveal
significant results at α < 0.1. Densities of Rotifera, Daphnia spp., other Cladocera taxa,
and total zooplankton increased with increasing soluble silica concentration, however the
regression models explained only little of the variability (Rotifera: r2 = 0.23, P = 0.03;
Daphnia: r2 = 0.2, P = 0.05; other Cladocera: r2 = 0.23, P = 0.03; total zooplankton: r2 =
0.19, P = 0.05) and there was no significant relationship between Copepoda density and
any of the measured variables.
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Benthic invertebrates
Taxa found in benthic invertebrate samples that were previously reported as
potential prey for age-0 pallid sturgeon included Chironomidae larvae and larvae of the
Ephemeroptera families Caenidae and Ephemeridae. Other taxa that were reported as
potential prey for age-0 pallid sturgeon, such as Amphipoda, Trichoptera, Diptera larvae
other than Chironomidae, and Ephemeroptera larvae in the family Baetidae were only
observed in low densities or at few sites and no statistical analyses were performed on
individual taxa, but were included in the comparison of total benthic invertebrate density.
Stovepipe samples
Mean Chironomidae, Caenidae, and Ephemeridae larvae densities in stovepipe
samples did not differ between habitat types, but significant differences were observed
for total benthic invertebrate density. Mean total benthic invertebrate density tended to be
higher at backwater habitats compared to all other habitat types, however post-hoc tests
were not significant at α < 0.1.
The best predictor variable for Chironomidae larvae density was total phosphorus
at which sites with higher Chironomidae larvae density had a higher total phosphorus
concentration (r2 = 0.49, P < 0.01). Variability in Caenidae larvae density was best
explained by velocity and macrophyte density at which Caenidae larvae density increased
with decreasing velocity and increasing macrophyte density (r2 = 0.63, P < 0.01). The
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best predictor variables for Ephemeridae larvae density were chlorophyll α concentration
and proportion of clay and silt (grain size < 0.063 mm) in the river sediment at which
Ephemeridae larvae density increased with increasing chlorophyll α concentration and
increasing proportion of clay and silt in the river sediment (r2 = 0.53, P < 0.01).
Variability in total benthic invertebrate density was best explained by velocity and
chlorophyll α concentration at which total benthic invertebrate density increased with
decreasing velocity and increasing chlorophyll α concentration (r2 = 0.50, P < 0.01).
D-frame net samples
Mean Chironomidae and Caenidae larvae densities were similar among habitat
types. Mean Ephemeridae larvae density differed among habitat types and tended to be
higher in backwater and side channel habitats compared to headwater and main channel
habitats, however post-hoc tests were not significant at α < 0.1. Mean total benthic
invertebrate density was significantly higher in backwater habitats compared to
headwater and main channel habitats.
No regression model was generated for Chironomidae larvae density and
Ephemeridae larvae density as there was no significant relationship with any of the
measured variables. Variability in Caenidae larvae density was best explained by velocity
and macrophyte density at which Caenidae larvae density increased with decreasing
velocity and increasing macrophyte density (r2 = 0.51, P < 0.01). Variability in total
benthic invertebrate density was best explained by macrophyte density at which total
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benthic invertebrate density increased with increasing macrophyte density (r2 = 0.48, P <
0.01).
Pallid sturgeon
Mean pallid sturgeon growth did not differ among habitat types or the laboratory
reference baseline (ANOVA, F = 1.178, df = 4, P = 0.35; Figure 2). Mean ± SE growth
pooled over all sites was 2.1 ± 0.45 mm and for the laboratory reference baseline was 3.0
± 0.37 mm. Similarly, mean energy density did not differ significantly among habitat
types or the laboratory reference baseline and was similar to the energy density at the
beginning of the experiment (ANOVA, F = 1.985, df = 5, P = 0.10, Figure 3). Mean ± SE
energy density pooled over all sites was 2514.58 ± 53.44 J/g wet weight, for the
laboratory reference baseline was 2639.10 ± 46.73 J/g wet weight, and initial energy
density was 2371.30 ± 51.59 J/g wet weight. Growth and energy density were variable
among individual sites and both variables were neither in the field (correlation coefficient
r = -0.242, P = 0.30) nor in the laboratory (correlation coefficient r = -0.085, P = 0.83)
correlated. Mortality was low during the study and survival rates did not differ
significantly among habitat types (Kruskal-Wallis-H, χ2 = 3.807, df = 3, P = 0.28). Mean
± SE survival rates were 86.6 ± 13.4 % for backwater habitats, 100 % for headwaters and
main channels habitats, and 86.8 ± 8.1 % for side channel habitats.
Overall, 75 % of pallid sturgeon had prey present in their digestive tract and no
significant differences in proportion of pallid sturgeon that consumed prey were observed
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between habitat types (Kruskal-Wallis-H, χ2 = 2.862, df = 3, P = 0.41). Chironomidae
larvae were the most frequently observed prey type in the digestive tract of pallid
sturgeon and accounted for 92.8 % of all ingested prey items. Chironomidae larvae were
consumed at 80 % of the headwater habitats, 60 % of the main channel habitats, 40 % of
the side channel habitats, and 20 % of the backwater habitats. Other identifiable prey
types included Ephemeroptera larvae (2.4 %), Amphipoda (2.4 %), and Corixidae (2.4
%). However, prey could only be identified from 37.1 % of fish with prey present (i.e.,
27.7 % of all fish), while for the majority of fish advanced digestion of prey items made
identification impossible.
To further investigate patterns between sites that fostered high and low growth
and energy density, pallid sturgeon were regrouped at which the cluster analysis revealed
a two cluster solution for both variables (hereafter referred to as high and low growth and
high and low energy density). Thirteen sites provided high growth and 7 sites provided
low growth. Among the sites that resulted in high growth were 3 backwater sites, 3
headwater sites, 3 main channel sites, and 4 side channel sites. Mean ± SE growth at sites
that fostered high growth was 2.82 ± 0.6 mm and at sites that fostered low growth was
0.81 ± 0.24 mm. However, abiotic variables (Tables 7 to 9), mean chlorophyll a
concentration (high growth, mean ± SE: 23.04 ± 1.66 μg/L; low growth, mean ± SE:
19.66 ± 1.66 μg/L; t-test, t = 1.359, df = 18, P = 0.19), mean macrophyte density (Mann-
Whitney-U test: Z = 0.000, P = 1.0), and mean zooplankton and benthic invertebrate
densities (Tables 10 to 12) did not differ between high and low growth sites. Furthermore
no differences in survival (high growth, mean ± SE: 92.3 ± 5.6 %; low growth, mean ±
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SE: 94.5 ± 5.5 %; Mann-Whitney-U test, Z = -0.128, P = 0.90) and percentage of fish that
had consumed prey (high growth, mean ± SE: 78.2 ± 7.2 %; low growth, mean ± SE:
69.0 ± 15.6 %; Mann-Whitney-U test, Z = -0.392, P = 0.76) were observed between sites
that fostered high and low growth.
Fish from 14 sites had high energy densities and fish from 6 sites had low energy
densities. High energy densities were found in pallid sturgeon from 5 backwater sites, 3
headwater sites, 3 main channel sites, and 3 side channel sites. Mean ± SE energy density
at sites that fostered high energy densities was 2621.87 ± 52.89 J/g wet weight and at
sites that resulted in low energy density was 2264.24 ± 35.99 J/g wet weight. Habitat
characteristics differed between low and high energy density sites. Velocity was lower
and mean sediment grain size was smaller at sites that resulted in high energy density
(Table 13), but no differences were observed between water quality variables (Table 14)
and nutrient concentrations (Table 15). Mean macrophyte densities were higher at high
energy density sites (Mann-Whitney-U test, Z = -1.835, P = 0.09), but mean chlorophyll
a concentrations were similar (high energy density, mean ± SE: 22.87 ± 1.61 μg/L; low
energy density, mean ± SE: 19.48 ± 2.67μg/L; Mann-Whitney-U test, Z = -1.072, P =
0.28). High energy density sites had higher mean densities of several zooplankton taxa
(i.e., Rotifera, Copepoda, Cladocera) and total zooplankton (Table 16). In addition, mean
Caenidae larvae density and total benthic invertebrate density in stovepipe and D-frame
net samples were higher at high energy density sites (Tables 17 and 18). Survival rates
were similar between high and low energy density sites (high energy density, mean ± SE:
90.0 ± 5.8 %; low energy density, mean ± SE 100 %; Mann-Whitney-U test, Z = -1.195,
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P = 0.23) and no differences in percentage of fish that consumed prey were observed
between sites that fostered high and low growth (high energy density, mean ± SE: 75.0 ±
8.9 %; low energy density, mean ± SE: 75.0 ± 12.0 %; Mann-Whitney-U test, Z = -
0.136, P = 0.90).
No regression model was generated for pallid sturgeon growth as there was no
significant relationship with any of the measured variables. Variability in energy density
was best explained by Caenidae larvae density from D-frame net samples and
Ephemeridae larvae density from stovepipe samples at which pallid sturgeon energy
density increased with increasing Caenidae and Ephemeridae larvae densities (r2 = 0.42,
P = 0.01).
DISCUSSION
Chlorophyll α concentration and macrophyte density
Mean chlorophyll α concentration across all sampling sites (mean ± SE: 21.86 ±
1.21 μg/L) was similar to concentrations observed by Fincel (2011) and Beaver et al.
(2013) in the sampling area, but considerably higher than those reported by Havel et al.
(2009; mean ± SE: 4 ± 0.4 μg/L) for the upper and middle Missouri River including the
Fort Randall Reach. Fincel (2011) reported a gradient of chlorophyll α concentrations
within the Fort Randall Reach at which the chlorophyll α concentration was low in the
free flowing upper part of the reach, increased in the Lewis and Clark Delta and
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continued to rise in Lewis and Clark Lake. As such considerably higher chlorophyll α
concentration in the present study compared to those observed by Havel et al. (2009) who
sampled the free flowing stretch of the Fort Randall Reach may be due to the downstream
sampling location in the Lewis and Clark Delta and the headwater of Lewis and Clark
Lake. We observed a higher chlorophyll a concentration at backwaters habitats compared
to main channel habitats, which was similarly reported in other studies (Wahl et al. 2008,
Burdis and Hoxmeier 2011, Dzialowski et al. 2013), but this is not obligate as
phytoplankton growth is affected by other variables, such as nutrient availability, river
connectivity and water residence time (Knowlton and Jones 2003, Limberger et al. 2004)
and Burdis and Hoxmeier (2011) did not observe higher chlorophyll α concentrations in
all sampled backwaters. Chlorophyll α concentration was positively correlated with total
phosphorus and negatively correlated with nitrate-N concentrations. A positive
correlation of chlorophyll α and total phosphorus concentrations was documented for
many lakes and rivers at which the strength of the relationship is influenced by
environmental factors, particularly water residence time (Søballe and Kimmel 1987). The
relationship of chlorophyll α and nitrate-N concentrations in contrast was negative.
Highest chlorophyll α concentrations were observed at two backwater sites (33.88 μg/L
and 30.15 μg/L) and one side channel site (30.07 μg/L), where nitrate-N concentrations
were as low as 0.2 mg/L for both backwater sites and 0.6 mg/L for the side channel site.
In addition to high chlorophyll α concentrations, macrophytes were present at each of
these sites. All three sites were located in the center of the Lewis and Clark Delta. In
contrast, a backwater site with a high chlorophyll α concentration (28.30 μg/L) and
macrophyte cover of 26 to 50 %, which was in close proximity to the South Dakota main
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channel, had a nitrate-N concentration (1.4 mg/L) similar to main channel sites (mean ±
SE: 1.32 ± 0.08). It was shown for the upper Mississippi River that nitrate concentrations
decrease with increasing distance to the nearest channel during low flow conditions due
to rapid nitrate depletion through nitrate uptake by algae and macrophytes and
denitrification in the sediment under anoxic conditions (Houser and Richardson 2010).
As such, low nitrate-N concentrations in presence of high chlorophyll α concentrations
and macrophyte densities may have been a result of assimilation or denitrification in
anoxic sediment layers accompanied by insufficient replenishment.
Macrophytes were present at all backwater sites and three side channel sites.
While also present at three main channel sites, densities were low and macrophytes were
absent from all but one headwater site. In fluvial environments significant macrophyte
growth is generally observed in shallow areas with sufficient light penetration, low
velocity and stable substrate (Peltier and Welch 1969, Chambers et al. 1991, Madsen et
al. 2001). Although velocities were low at the specific main channel sampling sites, likely
influenced by the low water levels during the sampling period, general velocities in the
main channel are higher and more variable, which may also decrease light penetration
through suspended sediment (Peltier and Welch 1969), and collectively limit macrophyte
growth. In agreement with our results, Galat et al. (2005) reported a near absence of
macrophytes from the Missouri River main channel. Highest velocities were observed at
headwater sites, which may have contributed to the absence of macrophytes at most sites.
Best predictor variables for macrophyte density were water depth and velocity, at which
macrophyte density was positively correlated with water depth and negatively correlated
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with velocity. The effect of velocity on macrophyte growth agrees with other studies as
mentioned above (Peltier and Welch 1969, Chambers et al. 1991, Madsen et al. 2001).
The positive relationship with water depth was likely an effect of habitat type
characteristic and generally low water depth at all sampling sites as macrophyte growth is
limited to the photic zone, and light penetration is among the limiting factors in the
Missouri River (Galat et al. 2005). Backwaters and three side channels had significant
macrophyte densities and sampling sites in both habitat types tended to be deeper than
main channel or headwater sampling sites where macrophytes were rare or only present
in low densities, which may explain the positive relationship.
The significance of primary productivity for higher trophic levels is well
established. Algae and higher plants provide food resources for many invertebrate taxa
(Thorp and Covich 2010) and the importance of macrophytes as habitat including their
significance as refuge from predation for zooplankton and benthic invertebrates has been
addressed (Newman 1991, Schriver et al. 1995). In addition, macrophytes are critical
components for many aquatic insects to complete their life cycle and several authors
emphasized their role for oviposition and emergence (McLaughlin and Harris 1990, Orr
and Resh 1992). Collectively, it was shown that algae and higher aquatic plants can be
important determinants for invertebrate spatial distribution (Scheffer et al. 1984, Whatley
et al. 2014). Similarly, algae and higher plants constitute food resources for herbivorous
fishes and macrophytes constitute important habitat for juvenile and adult fishes, serve as
nurseries and refuge for early life stages, and provide spawning and nesting substrate
(Petr 2000).
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Zooplankton
Mean total zooplankton density across all sampling sites (mean ± SE: 8.04 ± 2.99
individuals/L) was substantially lower in the Lewis and Clark Delta than has been
reported for many other large river ecosystems including other reaches of the Missouri
River (Dettmers et al. 2001, Wahl et al. 2008, Havel et al. 2009, Burdis and Hoxmeier
2011, Dzialowski et al. 2013). Observed zooplankton densities were also lower than
previously reported for the Fort Randall Reach during summer month (Fincel 2011), but
similar to the observed density at the Missouri River and Niobrara River confluence
(Havel et al. 2009). Low zooplankton densities may at least partially be related to the
sampling period during September. Zooplankton shows a high seasonality and densities
typically peak during the spring and summer and decline thereafter (Wahl et al. 2008,
Burdis and Hoxmeier 2011). As such, it may be possible that the zooplankton densities
observed in the present study reflect lower densities during early fall. Furthermore, the
zooplankton composition in other studies was often dominated by high Rotifera densities
which represented as much as over 90 % of the composition (Dettmers et al. 2001, Wahl
et al. 2008, Burdis and Hoxmeier 2011, Dzialowski et al. 2013). Rotifera densities
observed in the Lewis and Clark Delta were low and zooplankton was mainly composed
of Copepoda and Cladocera, which was reported by other authors for the middle Missouri
River and differs significantly from the lower Missouri River where Rotifera dominate
the zooplankton composition (Havel et al. 2009, Beaver et al. 2013). Densities of most
zooplankton taxa were higher in backwater habitats, although pairwise comparisons did
not reveal significant differences for all taxa with significant ANOVA models at α < 0.1.
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Particularly Daphnia spp. were more abundant and the mean density was about 10 times
higher in backwaters than in other habitat types. Higher zooplankton densities in
backwaters of large rivers compared to main channel and side channel habitats were
reported in other studies (Burdis and Hoxmeier 2011, Fisher 2011, Dzialowski et al.
2013) and it was suggested that longer water retention time, less turbulence, lower
velocity, and lower turbidity may benefit zooplankton, particularly Cladocera taxa
(Vranovský 1995, Schiemer et al. 2001, Burdis and Hoxmeier 2011). However, higher
zooplankton densities in backwaters are not obligate as similar densities were observed in
backwater, side and main channel habitats in the Illinois River (Dettmers et al. 2001,
Wahl et al. 2008) and Wahl et al. (2008) suspected significant main channel reproduction.
Soluble silica was the only variable that was significantly correlated with densities of
Rotifera, Daphnia spp. and other Cladocera as well as total zooplankton. However, for all
taxa soluble silica only explained little of the variation in zooplankton taxa and total
zooplankton densities. Rotifera, Daphnia spp. and other Cladocera as well as total
zooplankton densities were higher in backwater habitats, which also had a higher mean
soluble silica concentration and as such soluble silica may rather be a correlate of
zooplankton taxa and total zooplankton densities without direct causality. In contrast,
mean Copepoda density did not differ significantly between habitat types and there was
also no significant relationship between Copepoda density and any of the measured
variables, which supports the notion that the correlation between soluble silica and other
zooplankton taxa and total zooplankton densities may rather reflect a habitat type (i.e.,
backwater) effect. Similarly, Beaver et al. (2013) did not observe a strong correlation
between nutrient concentrations and zooplankton densities in the Missouri River reservoir
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system, but rather with other variables, such as water residence time, temperature and
water clarity.
Higher zooplankton densities in backwaters could benefit many fishes in the
Missouri River of which over 60 species are reported to feed on zooplankton during their
life (Wildhaber et al. 2011). These include early life stages of recreationally important
species in the Lewis and Clark Delta, such as walleye Sander vitreus and smallmouth
bass Micropterus dolomieu (Nunn et al. 2012), but also planktivorous species such as
paddlefish Polyodon spathula (Wildhaber et al. 2011). Furthermore zooplankton
constitutes an adequate prey resource for larval pallid sturgeon at the transition from
endogenous to exogenous feeding (Rapp Chapter II) and particularly Daphnia spp. were
frequently consumed by larvae during the first weeks of their life in laboratory prey
selection trials (Rapp Chapter III). Thus, higher zooplankton densities in backwaters
suggest that this habitat type could constitute important nurseries for early life stages of
many fishes in the Missouri River and, due to zooplankton drift into other habitats
(Vranovský 1995, Schiemer et al. 2001, Fisher 2011), may also benefit species which are
not directly using backwater habitats.
Benthic invertebrates
Mean densities of total benthic invertebrates, which were reported as prey for
larval and juvenile pallid sturgeon and Scaphirhynchus spp. (Braaten et al. 2012, Sechler
et al. 2012, 2013, Harrison et al. 2014) differed significantly between habitat types and
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tended to be higher in backwater habitats, although pairwise comparisons in significant
ANOVA models were not significant at α < 0.1 for stovepipe samplers. The most
frequently observed benthic invertebrates in stovepipe samplers and D-frame nets were
larvae of the two Ephemeroptera families Caenidae and Ephemeridae. In addition,
Chironomidae larvae were observed at many sites but densities were generally low. Other
taxa that constitute potential prey for pallid sturgeon were only observed at few sites or in
low densities (i.e., Amphipoda, Trichoptera larvae, Baetidae larvae, and Diptera larvae
other than Chironomidae larvae; Braaten et al. 2012, Sechler et al. 2012, 2013, Harrison
et al. 2014). Benthic invertebrate densities were considerably lower than those observed
in other rivers or reaches of the Missouri River (Grohs 2008, Peters et al. 1989, Galat et
al. 2005) and Ephemeroptera and Chironomidae larvae densities were slightly lower than
those observed during the fall in shallow water habitats in the Lewis and Clark Delta near
Springfield, SD in 2005 (Ephemeroptera larvae, mean ± SE: 73.61 ± 42.51/m2;
Chironomidae larvae, mean ± SE: 12.50 ± 7.31/m2) and 2006 (Ephemeroptera larvae,
mean ± SE: 19.44 ± 5.78/m2; Chironomidae larvae, mean ± SE: 16.67 ± 5.07/m2; Grohs
unpublished data). Lower densities may partially be explained by the different sampling
gears. Grohs (2008) used surber samplers in shallow water habitats, while in the present
study stovepipe samplers and D-frame nets were used due to generally low velocities at
the sampling sites during the study period, which made the use of surber samplers
impractical. Similar to the study by Grohs (2008), we observed high variability in benthic
invertebrate densities between sampling sites. For both sampling gears, Caenidae larvae
density increased with decreasing velocity and increasing macrophyte density.
Ephemeridae larvae density in stovepipe samples increased with increasing chlorophyll α
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concentration and increasing proportion of clay and silt in the river sediment. These
habitat associations generally agree with reported habitat preferences of the two families.
Caenidae larvae are typically found in lentic and stagnant or slow flowing lotic
environments in association with plants or leaf litter, while Ephemeridae larvae are
burrowers and found in association with fine sediment, such as clay and silt (Edmunds Jr.
et al. 1976). The best predictor variable for Chironomidae larvae density was total
phosphorus, which was similarly reported by other authors (e.g., Brooks et al. 2001,
Watzbinski and Quinlan 2013). Total benthic invertebrate density increased in stovepipe
samples with decreasing velocity and increasing chlorophyll α concentration and
increased in D-frame net samples with increasing macrophyte density.
Overall, the predictor variables for benthic invertebrate densities suggest that
particularly velocity, proportion of fines in the river sediment (i.e., clay, silt), chlorophyll
α concentration, and macrophyte density were important to explain variation in benthic
invertebrate densities in the Lewis and Clark Delta. The importance of algae and
macrophytes as food source and habitat for benthic invertebrates was addressed above. In
addition, macrophytes can decrease the flow velocity within beds and in adjacent areas
(Gregg and Rose 1985, Madsen et al. 2001) and may facilitate settlement of benthic
invertebrate taxa which are associated with stagnant water or moderate current velocities
such as Caenidae larvae (Edmunds Jr. et al. 1976). In fact, Gregg and Rose (1985)
considered velocity reduction the most important attribute for macrophyte and benthic
invertebrate associations. For the Missouri River below Gavins Point Dam, highest
benthic invertebrate densities were reported for Typha marshes, while lowest densities
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were reported for main channel habitats and non-vegetated side channels (Patrick 1998).
This is in agreement with the present study as we observed generally low benthic
invertebrate densities at main channel sites, the two un-vegetated side channel sites
(stovepipe sampler: 1.1 individuals/m2, D-frame net: 4.6 individuals/sweep) and
headwater sites, which were largely void of macrophytes. Galat et al. (2005) reported
increasing benthic invertebrate densities with increasing substrate stability, reduced
velocity and increasing silt and organic matter. Highest benthic invertebrate densities
were reported for hard substrates (e.g., snags or rocks; Benke et al. 1985, Peters et al.
1989, Galat et al. 2005), which we couldn’t test in the present study as neither of the
sampling sites had significant amounts of drift wood or rocks.
A combination of low velocity, fine sediment, high chlorophyll α concentration
and significant macrophyte density was observed at most backwater sites and three side
channel sites, while other sites were lacking one or more of these attributes. Backwaters
and side channels represent typical shallow water habitat features of floodplain-river
channel systems (Hesse and Sheets 1993, Baylay 1995) and can contribute to large
portions of the total invertebrate production (Thorp 1992, Thorp and Delong 1994, Ward
and Stanford 1995). Benthic invertebrates, in turn, constitute important prey resources for
many fishes and are the main prey for larval and juvenile pallid sturgeon (Wanner et al.
2007, Grohs et al. 2009, Braaten et al. 2012). Thus, habitats that mimic floodplain-river
channel system characteristics such as vegetated backwaters and side channels may
benefit a variety of fishes in the modified Missouri River ecosystem either through direct
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use of these habitats or indirectly through spread and drift of benthic invertebrates into
other habitats.
Pallid sturgeon
Mean growth was similar among habitat types but variable among individual
sites. Growth ranged from 0 to 9.5 mm for individual sites during the study period and as
such was lower than previously reported for age-0 pallid sturgeon and Scaphirhynchus
spp. from other reaches of the Missouri River (Phelps et al. 2010, Braaten et al. 2012).
Lower growth compared to other studies may be explained by origin (e.g., maternal
contribution) or sampling season. Our study was conducted during September when mean
± SD water temperatures were 21.79 ± 0.39˚C while other studies estimated growth of
age-0 pallid sturgeon or Scaphirhynchus spp. over summer when water temperatures
were higher (e.g., mean: 23.5˚C, Braaten et al. 2012) and included periods of high water
temperatures. Water temperature is a determining variable for growth (Schiemer et al.
2001, 2002) and it was reported that differences in water temperature can result in
pronounced effects on growth of pallid sturgeon (D. Deslauriers personal communication,
South Dakota State University, L. Heironimous personal communication, South Dakota
State University). Furthermore, Le Pape and Bonhommeau (in press) discussed potential
overestimation of growth from field studies as fast growing individuals are more likely to
survive while slow growing individuals are more likely to be removed from the
population due to size and growth selective mortality and thus fast growing fish can be
126
overrepresented in the sample. Similar growth between the laboratory reference baseline
and the field study suggests that lower growth rates were likely not a result of unsuitable
conditions in the Lewis and Clark Delta. However, we may have slightly underestimated
growth in the laboratory as fish were incubated at 20˚C and as such water temperature in
the laboratory was slightly cooler than during the field study, where the mean
temperature ranged among sites from 21.0°C to 22.2°C. In addition to growth, we
assessed energy density of pallid sturgeon. Mean energy density did not differ between
habitat types and the laboratory reference baseline and was not significantly different
from the initial condition. Mean energy density observed in the present study was higher
than reported for age-0 Scaphirhynchus spp. ≤ 50 mm, but lower than reported for fish
ranging from 51 to 200 mm in the middle Mississippi River (Sechler et al. 2012). Energy
density increases with increasing fish size (Pothoven et al. 2006, 2012) and pallid
sturgeon in the present study (final mean ± SD fork length: 69.9 ± 2.4 mm) were larger
than small fish used by Sechler et al. (2012), but at the lower end of the range for large
fish. As such, the mean energy density observed in the present study may have been
comparable to the energy density of Scaphirhynchus spp. in the middle Mississippi River.
Due to high variability within habitat types and differences among individual
sites, we dropped the habitat type-specific analysis and clustered sites in those that
fostered high and low growth and energy density, respectively. While we did not find
significant differences in any measured variable between sites that resulted in high and
low growth and regression analysis did not reveal a significant relationship between
growth and any of the measured variables, we found differences for sites that fostered
127
high and low energy densities. It was revealed that sites at which fish had high energy
densities had lower velocity, smaller mean sediment grain size, higher macrophyte
density, higher densities of all zooplankton taxa except for Daphnia spp., higher
Caenidae larvae density, and higher total benthic invertebrate density that constitute
common prey for pallid sturgeon. As previously discussed, velocity, proportion of fines
in the river sediment (i.e., clay, silt), and macrophyte density were among the best
predictor variables for benthic invertebrate densities. In turn, regression analysis revealed
high Caenidae and Ephemeridae larvae densities as best predictors for high energy
densities in pallid sturgeon. Thus, it seems likely that habitat conditions that favor benthic
invertebrates, particularly Ephemeroptera larvae, could ultimately improve pallid
sturgeon condition. However, with regard to the importance of Ephemeroptera larvae we
did not find direct support for this assumption in the diet analysis as prey from 62.9 % of
fish with prey present could not be identified due to advanced digestion. Of the
identifiable prey items 92.8 % were Chironomidae larvae and could be identified by the
presence of head capsules likely due to their long digestion time (Gannon 1976).
Chironomidae larvae were frequently reported as integral prey for pallid sturgeon in field
studies and pallid sturgeon selected for Chironomidae larvae over Ephemeroptera larvae
in a laboratory study (Rapp Chapter II). However, laboratory experiments suggest that
pallid sturgeon feed opportunistically and it was documented that the proportion of
Ephemeroptera larvae in the diet increases when available in high densities and
Chironomidae larvae, in turn, are only available in low densities (Rapp Chapter II) as it
was the case during the study period in the Lewis and Clark Delta. As such, despite the
lack of direct evidence from pallid sturgeon diets, one could hypothesize that
128
Chironomidae larvae were overrepresented in diet due to differential digestion time of
prey items, particularly the long digestion time for Chironomidae larvae head capsules
(Gannon 1976), and unidentifiable diet items included Ephemeroptera larvae, which were
the most frequently observed benthic invertebrate taxa.
Conclusions
We observed high heterogeneity within habitat types for many variables and each
trophic level and there was no evidence for the general superiority of one habitat type
over another with regard to their suitability as nursery habitats for age-0 pallid sturgeon.
However, backwaters supported higher zooplankton densities, which could benefit larval
pallid sturgeon for which zooplankton is an appropriate prey resource (Rapp Chapter II)
or other fishes as most species are planktivorous during their early life history (Nunn et
al. 2012) or even throughout their life (e.g., paddlefish, Wildhaber et al. 2011). Densities
of the most common benthic invertebrate taxa did not significantly differ between habitat
types, except for D-frame net samples of Ephemeridae larvae, but backwaters had higher
total benthic invertebrate densities which constitute potential prey for pallid sturgeon and
Scaphirhynchus spp. (Braaten et al. 2012, Sechler et al. 2012, 2013, Harrison et al. 2014).
Benthic invertebrate taxa densities and total benthic invertebrate density were
significantly correlated with only few variables which included velocity, proportion of
clay and silt in the river sediment, chlorophyll α concentration, and macrophyte density.
As such habitats that provide low velocities, fine substrate, high algal biomass and high
129
macrophyte density could foster high benthic invertebrate densities, which provide
important prey resources for pallid sturgeon and other fishes in the Missouri River
ecosystem.
Pallid sturgeon energy density was significantly correlated with Caenidae larvae
densities from D-frame net samples and Ephemeridae larvae density from stovepipe
samples. Caenidae larvae density increased with decreasing velocity and increasing
macrophyte density and Ephemeridae larvae density increased with increasing
chlorophyll а concentration and increasing proportion of clay and silt in the river
sediment. The combination of these attributes was observed in most backwater habitats
and at three side channel sites, while other sites were lacking one or more of these
characteristics. Pallid sturgeon energy density differences were particularly pronounced
between side channel sites and were amongst the highest observed in the present study
for the three side channels sites with high macrophyte densities (i.e., 25 to 75 %
macrophyte cover) and fine substrate (mean: 2767.34 J/g wet weight) and were amongst
the lowest for the two side channel sites that were void of macrophytes and where the
substrate was dominated by coarser fractions (mean: 2205.28 J/g wet weight).
Furthermore, a recent study suggests that macrophyte cover plays an important role for
early life stage spatial distribution of the sympatric shovelnose sturgeon (Hinz et al. in
press).
Collectively, the results of this study support the conservation and rehabilitation
of shallow water habitat as a tool for pallid sturgeon recovery. However, the specific
habitat type (e.g. backwater, side channel, etc.) is less important and emphasis of habitat
130
creation should be placed towards low velocity habitats with fine substrate suitable for
macrophyte colonization and enhanced algal production, which foster benthic
invertebrate colonization and may ultimately benefit pallid sturgeon.
ACKNOWLEDGEMENTS
Funding for this study was provided by the US Army Corps of Engineers. We
thank the hatchery personnel at Garrison Dam National Fish Hatchery for providing
pallid sturgeon and the personnel at Gavins Point Dam National Fish Hatchery for
logistic support. Field and laboratory assistance was provided by Jake Mecham, Mark
Kaemingk, Eli Felts, Tanner Stevens, Andrew Carlson, Erinn Ipsen, Jason Augspurger,
Tanner Brouwer, Thomas Larson, Jacob Schwoerer, and Tyler Trimpe. We thank
Michael Brown and Prairie Aqua Tech for support with bomb calorimetry and water
sample analyzes.
131
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Table 4-1: Physical habitat characteristics for habitat types in the Lewis and Clark Delta. Habitat types include backwaters, Lewis and
Clark Lake headwaters, main channel depositional zones, and side channels. Presented results are means ± SE. Calculated F-values
refer to ANOVA results. Different letters indicate significant differences. Significance was assessed at P < 0.1.
Variable Backwater
Lewis and Clark
Lake Headwater
Main channel
Side channel
F-value, df, P-value
Depth (cm) 61.66 ± 4.17yz 56.68 ± 2.39z 55.20 ± 0.66z 68.06 ± 4.20y F = 3.279, df = 3, P =
0.05
Velocity (cm/s)
2.0 ± 0.9z 9.8 ± 2.3y 2.6 ± 0.6z 6.0 ± 1.9yz F = 5.117, df = 3, P =
0.01
Grain size
(geometric mean,
μm)
93.63 ± 13.91z 221.78 ± 12.78y 66.21 ± 16.06z 122.33 ± 34.60yz F = 10.164, df = 3, P
= 0.001
Total volatile solids
(sediment, %)
2.3 ± 0.66yz 0.95 ± 0.22z 3.13 ± 0.74y 1.68 ± 0.31yz F = 3.626, df = 3, P =
0.04
145
Table 4-2: Water quality variables for habitat types in the Lewis and Clark Delta. Habitat types include backwaters, Lewis and Clark
Lake headwaters, main channel depositional zones, and side channels. Presented results are means ± SE. Calculated F-values refer to
ANOVA results and χ2-values to Kruskal-Wallis-H test results. Different letters indicate significant differences. Significance was
assessed at P < 0.1.
Variable Backwater Lewis and Clark
Lake Headwater
Main channel Side channel F-value or χ2-value,
df, P-value
Temperature (C˚) 21.31 ± 0.18 22.01 ± 0.15 21.91 ± 0.10 22.02 ± 0.10 χ2 = 7.313, df = 3, P =
0.06
Dissolved oxygen
(mg/L)
7.75 ± 0.06 7.74 ± 0.059 7.80 ± 0.058 7.71 ± 0.22 χ2 = 1.543, df = 3, P =
0.67
pH 8.42 ± 0.046 8.5 ± 0.013 8.47 ± 0.019 8.46 ± 0.024 χ2 = 3.296, df = 3, P =
0.35
Salinity (ppm) 452.25 ± 0.75 450.80 ± 1.07 451.20 ± 1.32 450.20 ± 2.18 F = 0.308, df = 3, P =
0.82
Conductivity
(μS/cm)
819.0 ± 0.0 819.6 ± 1.4 819.2 ± 2.96 815.40 ± 3.53 χ2 = 1.896, df = 3, P =
0.59
146
Turbidity (NTU) 12.10 ± 1.25 10.97 ± 0.57 9.15 ± 2.01 10.06 ± 1.48 χ2 = 3.829, df = 3, P =
0.28
Total dissolved
solids (ppm)
580.5 ± 0.65 579.6 ± 0.4 576.6 ± 3.14 578.4 ± 2.62 χ2 = 0.982, df = 3, P =
0.81
Total suspended
solids
(mg/L)
16.28 ± 2.50 20.60 ± 3.26 19.60 ± 0.80 13.37 ± 2.32 F = 1.898, df = 3, P =
0.17
Total volatile solids
(water, mg/L)
2.91 ± 0.37yz 3.09 ± 0.16z 3.03 ± 0.36yz 2.21 ± 0.20y χ2 = 6.954, df = 3, P =
0.07
147
Table 4-3: Nutrient concentrations for habitat types in the Lewis and Clark Delta. Habitat types include backwaters, Lewis and Clark
Lake headwaters, main channel depositional zones, and side channels. Presented results are means ± SE. Calculated F-values refer to
ANOVA results and χ2-values to Kruskal-Wallis-H test results. Different letters indicate significant differences. Significance was
assessed at P < 0.1.
Variable Backwater Lewis and Clark
Lake Headwater
Main channel
Side channel F-value or χ2-value,
df, P-value
Total nitrogen (mg/L) 1.78 ± 0.27 1.75 ± 0.38 1.85 ± 0.23 1.85 ± 0.21 F = 0.031, df = , P =
0.99
Nitrate-N (mg/L) 0.64 ± 0.22z 1.3 ± 0.13y 1.32 ± 0.08y 1.28 ± 0.21y F = 4.248, df = 3, P =
0.02
Nitrite-N (mg/L) 0.003 ± 0.0005yz 0.002 ± 0.0004z 0.004 ± 0.0003y 0.004 ± 0.0005y F = 5.638, df = 3, P =
0.01
Ammonia-N (mg/L) 0.066 ± 0.041 0.070 ± 0.006 0.072 ± 0.012 0.08 ± 0.012 χ2 = 0.831, df = 3, P =
0.84
Total phosphorus
(mg/L)
0.065 ± 0.007 0.061 ± 0.004 0.050 ± 0.004 0.054 ± 0.006 F = 1.674, df = 3, P =
0.21
148
Total dissolved
phosphorus (mg/L)
0.035 ± 0.006 0.033 ± 0.002 0.035 ± 0.003 0.031 ± 0.003 F = 0.197, df = 3, P =
0.90
Orthophosphate-P
(mg/L)
0.024 ± 0.005 0.021 ± 0.004 0.017 ± 0.004 0.017 ± 0.004 F = 0.611, df = 3, P =
0.62
Soluble silica (mg/L) 5.76 ± 0.67y 4.36 ± 0.54yz 3.79 ± 0.67yz 2.98 ± 0.50z F = 3.824, df = 3, P =
0.03
149
Table 4-4: Zooplankton densities for habitat types in the Lewis and Clark Delta. Habitat types include backwaters, Lewis and Clark
Lake headwaters, main channel depositional zones, and side channels. Presented results are means ± SE. Calculated F-values refer to
ANOVA results. Different letters indicate significant differences. Significance was assessed at P < 0.1.
Variable Backwater
Lewis and Clark
Lake Headwater
Main channel
Side channel F-value, df, P-value
Rotifera
(Individuals/L)
2.47 ± 0.93 1.82 ± 0.51 0.57 ± 0.22 0.48 ± 0.09 F = 3.261, df = 3, P =
0.05
Copepoda
(Individuals/L)
5.88 ± 2.59 3.09 ± 1.21 1.59 ± 0.58 1.21 ± 0.14 F = 2.368, df = 3, P =
0.11
Daphnia
(Individuals/L)
10.07 ± 6.97y 1.0 ± 0.31z 0.55 ± 0.26z 0.77 ± 0.27z F = 5.462, df = 3, P =
0.01
Other Cladocera
(Individuals/L)
1.70 ± 0.62y 0.45 ± 0.20yz 0.22 ± 0.07yz 0.11 ± 0.06z F = 11.297, df = 3, P
= 0.01
Total Zooplankton
(Individuals/L)
20.28 ± 10.64 6.38 ± 1.75 2.94 ± 0.87 2.57 ± 0.46 F = 4.893, df = 3, P =
0.01
150
Table 4-5: Benthic invertebrate densities collected with stovepipe samplers for habitat types in the Lewis and Clark Delta. Habitat
types include backwaters, Lewis and Clark Lake headwaters, main channel depositional zones, and side channels. Presented results are
means ± SE. Calculated F-values refer to ANOVA results and χ2-values to Kruskal-Wallis-H test results. Different letters indicate
significant differences. Significance was assessed at P < 0.1.
Variable Backwater
Lewis and Clark
Lake Headwater
Main channel
Side channel
F-value or χ2-value,
df, P-value
Chironomidae
(Individuals/m2)
3.52 ± 1.79 1.76 ± 1.28 0.44 ± 0.44 1.32 ± 1.32 χ2 = 0.434, df = 3, P
= 0.43
Caenidae
(Individuals/m2)
20.22 ± 9.86 5.28 ± 3.0 6.15 ± 3.22 3.96 ± 2.01 F = 1.915, df = 3, P =
0.17
Ephemeridae
(Individuals/m2)
2.64 ± 1.62 0.88 ± 0.88 1.31 ± 0.88 1.31 ± 0.88 χ2 = 3.880, df = 3, P =
0.28
Total benthic
invertebrates
(Individuals/m2)
54.05 ± 24.91 8.79 ± 3.81 9.23 ± 3.22 10.99 ± 6.63 F = 2.922, df = 3, P =
0.07
151
Table 4-6: Benthic invertebrate densities collected with D-frame nets for habitat types in the Lewis and Clark Delta. Habitat types
include backwaters, Lewis and Clark Lake headwaters, main channel depositional zones, and side channels. Presented results are
means ± SE. Calculated F-values refer to ANOVA results. Different letters indicate significant differences. Significance was assessed
at P < 0.1.
Variable Backwater
Lewis and Clark
Lake Headwater
Main channel
Side channel F-value, df, P-
value
Chironomidae
(Individuals/sweep)
0.88 ± 0.39 0.68 ± 0.26 0.37 ± 0.26 0.28 ± 0.10 F = 0.926, df = 3, P
= 0.45
Caenidae
(Individuals/sweep)
4.72 ± 1.85 1.04 ± 0.28 2.0 ± 1.03 2.64 ± 0.94 F = 1.634, df = 3, P
= 0.22
Ephemeridae
(Individuals/sweep)
2.20 ± 0.80 0.60 ± 0.32 0.95 ± 0.32 3.32 ± 1.08 F = 3.078, df = 3, P
= 0.06
Total benthic invertebrates
(Individuals/sweep)
21.92 ± 6.79y 2.60 ± 0.29z 4.77 ± 3.69z 11.56 ± 4.84yz F = 4.174, df = 3, P
=0.02
152
Table 4-7: Physical habitat characteristics at sampling sites in the Lewis and Clark Delta
which supported low and high growth of pallid sturgeon. Presented results are means ±
SE. Calculated t-values refer to t-test results. Significance was assessed at P < 0.1.
Variable High growth Low growth t-value, df, P-value
Velocity (cm/s) 5.69 ± 1.4 4.0 ± 3.5 t = 783, df = 18, P =
0.44
Depth (cm) 61.63 ± 9.44 58.11 ± 5.82 t = 0.892, df = 18, P =
0.38
Mean grain size (μm) 126.10 ± 21.27 125.79 ± 76.08 t = 0.029, df = 18, P =
0.98
Total volatile solids
(sediment, %)
2.12 ± 0.43 1.82 ± 0.41 t = 0.359, df = 18, P =
0.72
153
Table 4-8: Water quality variables at sampling sites in the Lewis and Clark Delta which
supported low and high growth of pallid sturgeon. Presented results are means ± SE.
Calculated t-values refer to t-test results and Z-values refer to Mann-Whitney-U test
results. Significance was assessed at P < 0.1.
Variable High growth Low growth t-value or Z-value,
df, P-value
Temperature (C˚) 21.72 ± 0.14 21.89 ± 0.10 Z = -0.587, P = 0.56
Dissolved oxygen
(mg/L)
7.77 ± 0.03 7.72 ± 0.04 Z = -1.276, P = 0.20
pH 8.45 ± 0.02 8.50 ± 0.02 Z = -1.530, P = 0.13
Salinity (ppm) 450.46 ± 0.95 452.33 ± 0.72 Z = -1.202, P = 0.23
Conductivity (μS/cm) 817.54 ± 1.66 819.83 ± 1.52 Z = -0.575, P = 0.57
Turbidity (NTU) 9.88 ± 0.73 11.82 ± 1.54 t = -1.301, df = 17, P
= 0.21
Total dissolved solids
(ppm)
579.31 ± 1.07 577.33 ± 2.50 Z = -0.684, P = 0.49
Total suspended
solids (mg/L)
18.09 ± 1.21 16.29 ± 3.00 t = 0.664, df = 18, P =
0.52
Total volatile solids
(water, mg/L)
2.91 ± 0.20 2.64 ± 0.25 t = 0.797, df = 18, P =
0.44
154
Table 4-9: Nutrient concentrations at sampling sites in the Lewis and Clark Delta which
supported low and high growth of pallid sturgeon. Presented results are means ± SE.
Calculated t-values refer to t-test results. Significance was assessed at P < 0.1.
Variable High growth Low growth t-value, df, P-value
Total nitrogen (mg/L) 1.77 ± 0.15 1.87 ± 0.25 t = -0.344, df = 15, P
= 0.74
Nitrate-N (mg/L) 1.12 ± 0.14 1.17 ± 0.14 t = -0.255, df = 18, P
= 0.80
Nitrite-N (mg/L) 0.004 ± 0.0003 0.003 ± 0.0005 t = 1.070, df = 18, P =
0.30
Ammonia-N (mg/L) 0.077 ± 0.015 0.065 ± 0.011 t = 0.537, df = 14, P =
0.60
Total phosphorus
(mg/L)
0.060 ± 0.004 0.052 ± 0.004 t = 1.452, df = 18, P =
0.16
Total dissolved
phosphorus (mg/L)
0.035 ± 0.002 0.030 ± 0.002 t = 1.284, df = 18, P =
0.22
Orthophosphate-P
(mg/L)
0.018 ± 0.003 0.022 ± 0.003 t = -1.038, df = 18, P
= 0.31
Soluble silica (mg/L) 3.99 ± 0.47 4.66 ± 0.57 t = -0.896, df = 18, P
= 0.38
155
Table 4-10: Zooplankton densities at sampling sites in the Lewis and Clark Delta which
supported low and high growth of pallid sturgeon. Presented results are means ± SE.
Calculated Z-values refer to Mann-Whitney-U test results. Significance was assessed at P
< 0.1.
Variable High growth Low growth Z-value, df, P-value
Rotifera
(Individuals/L)
1.17 ± 0.37 1.63 ± 0.61 Z = -0.594, P = 0.55
Copepoda
(Individuals/L)
2.77 ± 1.10 3.26 ± 1.08 Z = -0.753, P = 0.45
Daphnia
(Individuals/L)
3.76 ± 2.84 1.86 ± 0.76 Z = -0.436, P = 0.66
Other Cladocera
(Individuals/L)
0.45 ± 0.20 0.94 ± 0.48 Z = -1.387, P = 0.17
Total Zooplankton
(Individuals/L)
8.22 ± 4.45 7.71 ± 2.64 Z = -0.911, P = 0.36
156
Table 4-11: Benthic invertebrate densities collected with stovepipe samplers at sampling
sites in the Lewis and Clark Delta which supported low and high growth of pallid
sturgeon. Presented results are means ± SE. Calculated t-values refer to t-test results and
Z-values refer to Mann-Whitney-U test results. Significance was assessed at P < 0.1.
Variable High growth Low growth t-value or Z-value,
df, P-value
Chironomidae
(Individuals/m2)
2.20 ± 0.86 0.94 ± 0.94 Z = -1.260, P = 0.21
Caenidae
(Individuals/m2)
9.98 ± 4.44 6.91 ± 1.94 t = -0.384, df = 18, P
= 0.71
Ephemeridae
(Individuals/m2)
1.69 ± 0.75 1.26 ± 0.65 Z = -0.045, P = 0.96
Total benthic
invertebrates
(Individuals/m2)
25.02 ± 11.33 13.19 ± 4.04 t = -0.339, df = 18, P
= 0.74
157
Table 4-12: Benthic invertebrate densities collected with D-frame nets at sampling sites
in the Lewis and Clark Delta which supported low and high growth of pallid sturgeon.
Presented results are means ± SE. Calculated t-values refer to t-test results and Z-values
refer to Mann-Whitney-U test results. Significance was assessed at P < 0.1.
Variable High growth Low growth t-value or Z-value,
df, P-value
Chironomidae
(Individuals/sweep)
0.54 ± 0.19 0.57 ± 0.19 Z = -0.846, P = 0.40
Caenidae
(Individuals/sweep)
2.60 ± 0.73 2.60 ± 1.21 t = 0.075, df = 18, P
= 0.94
Ephemeridae
(Individuals/sweep)
1.68 ± 0.40 1.94 ± 0.95 t = 0.123, df = 18, P
= 0.90
Total benthic
invertebrates
(Individuals/sweep)
10.57 ± 3.41 9.55 ± 4.27 Z = -0.555, P = 0.58
158
Table 4-13: Physical habitat characteristics at sampling sites in the Lewis and Clark
Delta which supported low and high energies density of pallid sturgeon. Presented results
are means ± SE. Calculated t-values refer to t-test results. Significance was assessed at P
< 0.1.
Variable High energy density Low energy density t-value, df, P-value
Velocity (cm/s) 3.9 ± 0.9 7.8 ± 2.4 t = -1.856, df = 18, P
= 0.08
Depth (cm) 60.99 ± 2.47 59.03 ± 2.61 t = 0.469, df = 18, P =
0.65
Mean grain size (μm) 106.94 ± 18.87 170.42 ± 68.68 t = -1.978, df = 18, P
= 0.06
Total volatile solids
(sediment, %)
2.30 ± 0.40 1.35 ± 0.37 t = 1.578, df = 18, P =
0.13
159
Table 4-14: Water quality variables at sampling sites in the Lewis and Clark Delta which
supported low and high energy densities of pallid sturgeon. Presented results are means ±
SE. Calculated t-values refer to t-test results and Z-values refer to Mann-Whitney-U test
results. Significance was assessed at P < 0.1.
Variable High energy density Low energy density t-value or Z-value,
df, P-value
Temperature (C˚) 21.75 ± 0.12 21.93 ± 0.07 Z = -0.170, P = 0.87
Dissolved oxygen
(mg/L)
7.76 ± 0.03 7.75 ± 0.04 Z = -0.440, P = 0.66
pH 8.46 ± 0.19 8.49 ± 0.08 Z = -0.630, P = 0.53
Salinity (ppm) 451.23 ± 0.98 450.67 ± 0.80 Z = -0.846, P = 0.40
Conductivity (μS/cm) 817.54 ± 1.70 819.83 ± 1.25 Z = -0.752, P = 0.45
Turbidity (NTU) 578.15 ± 1.53 579.83 ± 0.40 Z = -0.183, P = 0.86
Total dissolved solids
(ppm)
17.06 ± 1.77 18.40 ± 1.20 t = -0.473, df = 18, P
= 0.64
Total suspended
solids (mg/L)
2.88 ± 0.22 2.67 ± 0.11 t = 0.603, df = 18, P =
0.55
Total volatile solids
(water, mg/L)
10.96 ± 0.94 9.47 ± 0.91 t = 0.977, df =18, P =
0.34
160
Table 4-15: Nutrient concentrations at sampling sites in the Lewis and Clark Delta which
supported low and high energy densities of pallid sturgeon. Presented results are means ±
SE. Calculated T-values refer to t-test results. Significance was assessed at P < 0.1.
Variable High energy density Low energy density t-value, df, P-value
Total nitrogen
(mg/L)
1.83 ± 0.14 1.76 ± 0.29 t = 0.226, df = 15, P =
0.82
Nitrate-N (mg/L) 1.05 ± 0.13 1.31 ± 0.13 t = -1.173, df = 18, P
= 0.26
Nitrite-N (mg/L) 0.003 ± 0.0003 0.004 ± 0.0006 t = -1.032, df =18, P =
0.32
Ammonia-N (mg/L) 0.073 ± 0.014 0.070 ± 0.012 t = 0.135, df = 14, P =
0.90
Total phosphorus
(mg/L)
0.059 ± 0.004 0.054 ± 0.005 t = 0.757, df = 18, P =
0.46
Total dissolved
phosphorus (mg/L)
0.033 ± 0.002 0.033 ± 0.003 t = 0.068, df = 18, P =
0.95
Orthophosphate-P
(mg/L)
0.021 ± 0.002 0.015 ± 0.003 t = 1.483, df = 18, P =
0.16
Soluble silica (mg/L) 4.36 ± 0.43 3.91 ± 0.70 t = 0.561, df = 18, P =
0.58
161
Table 4-16: Zooplankton densities at sampling sites in the Lewis and Clark Delta which
supported low and high energy densities of pallid sturgeon. Presented results are means ±
SE. Calculated t-values refer to t-test results and Z-values refer to Mann-Whitney-U test
results. Significance was assessed at P < 0.1.
Variable High energy density Low energy density t-value or Z-value,
df, P-value
Rotifera
(Individuals/L)
1.66 ± 0.42 0.57 ± 0.92 t = 2.422, df = 16.372,
P = 0.03
Copepoda
(Individuals/L)
3.76 ± 1.06 1.03 ± 0.14 Z = -2.227, P = 0.03
Daphnia
(Individuals/L)
4.08 ± 2.6 0.79 ± 0.26 Z = -1.155, P = 0.25
Other Cladocera
(Individuals/L)
0.84 ± 0.28 0.10 ± 0.03 Z = -2.269, P = 0.02
Total Zooplankton
(Individuals/L)
10.42 ± 4.14 2.50 ± 0.79 t = 1.986, df = 18, P =
0.06
162
Table 4-17: Benthic invertebrate densities collected with D-frame nets at sampling sites
in the Lewis and Clark Delta which supported low and high energy densities of pallid
sturgeon. Presented results are means ± SE. Calculated t-values refer to t-test results and
Z-values refer to Mann-Whitney-U test results. Significance was assessed at P < 0.1.
Variable High energy density Low energy density t-value or Z-value,
df, P-value
Chironomidae
(Individuals/m2)
2.19 ± 0.89 0.73 ± 0.46 Z = -0.486, P = 0.63
Caenidae
(Individuals/m2)
11.77 ± 3.95 2.19 ± 1.39 t = 2.337, df = 18, P =
0.03
Ephemeridae
(Individuals/m2)
2.04 ± 0.71 0.37 ± 0.37 Z = -1.500, P = 0.13
Total benthic
invertebrates
(Individuals/m2)
27.94 ± 10.19 4.40 ± 2.05 t = 2.290, df = 18, P =
0.03
163
Table 4-18: Benthic invertebrate densities collected with D-frame nets at sampling sites
in the Lewis and Clark Delta which supported low and high energy densities of pallid
sturgeon. Presented results are means ± SE. Calculated t-values refer to t-test results and
Z-values refer to Mann-Whitney-U test results. Significance was assessed at P < 0.1.
Variable High energy density Low energy density t-value or Z-value,
df, P-value
Chironomidae
(Individuals/sweep)
0.55 ± 0.18 0.57 ± 0.20 Z = -0.503, P = 0.62
Caenidae
(Individuals/sweep)
3.39 ± 0.79 0.77 ± 0.28 Z = -2.360, P = 0.02
Ephemeridae
(Individuals/sweep)
1.85 ± 0.54 1.57 ± 0.57 t = 0.045, df = 18, P =
0.97
Total benthic
invertebrates
(Individuals/sweep)
12.88 ± 3.50 4.00 ± 0.70 t = 2.056, df =
17.847, P = 0.06
164
Figure 4-1: Sampling sites at the Lewis and Clark Delta. Red marks represent backwater
sites, orange marks represent Lewis and Clark Lake headwater sites, yellow marks
represent main channel depositional zones, and black marks represent side channel sites.
165
Gro
wth
(m
m)
0
1
2
3
4
5
6
Bas
elin
e
Bac
kwat
er
Hea
dwat
er
Mai
n ch
anne
l
Side ch
anne
l
Habitat type
Figure 4-2: Mean ± SE growth (mm) of age-0 pallid sturgeon in 4 different habitat types
in the Lewis and Clark Delta (open bars) and the laboratory reference baseline (closed
bar). Habitat types include backwaters, Lewis and Clark Lake headwaters, main channel
depositional zones, and side channels. (ANOVA, F = 1.178, df = 4, P = 0.35).
166
En
ergy d
en
sity
(J/g
wet
weig
ht)
0
500
1000
1500
2000
2500
3000
Initi
al
Bas
elin
e
Bac
kwat
er
Hea
dwat
er
Mai
n ch
anne
l
Side ch
anne
l
Habitat type
Figure 4-3: Initial (hatched bar) and final mean ± SE energy density (J/g wet weight) of
age-0 pallid sturgeon in 4 different habitat types in the Lewis and Clark Delta (open bars)
and the laboratory reference baseline (closed bar). Habitat types include backwaters,
Lewis and Clark Lake headwaters, main channel depositional zones, and side channels.
(ANOVA, F = 1.985, df = 5, P = 0.10).
167
CHAPTER V
SUMMARY
Our research addressed aspects of the larval and juvenile pallid sturgeon
Scaphirhynchus albus ecology, which was identified as important researches need
(Wildhaber et al. 2011). As part of this work we studied the foraging ecology of larval
and juvenile pallid sturgeon, which provides vital information for effective population
and community management with implications for habitat conservation and restoration
(Nunn et al. 2012). We assessed the transition from endogenous to exogenous feeding,
quantified growth and survival of larval pallid sturgeon in response to different prey
types (Chapter II) and conducted laboratory prey selection experiments to identify
important prey items for larval and juvenile pallid sturgeon (Chapter III). In a field study
we evaluated shallow water habitats in the Lewis and Clark Delta with particular focus on
their suitability as nurseries for pallid sturgeon (Chapter IV).
We assessed the transition from endogenous to exogenous feeding, which
represents a critical period for fishes during which high mortalities occur, with potentially
pronounced effects on recruitment (Larkin 1978). We did not observe a distinct mixed
endogenous and exogenous feeding period, which is considered to mitigate the transition
to exogenous feeding. The lack of a mixed feeding period may render pallid sturgeon
larvae particularly vulnerable to starvation if appropriate prey is rare and emphasizes the
importance of quality nursery habitats within the drift distance of pallid sturgeon in the
Missouri River. First prey ingestion was observed on the day of yolk sac absorption in
168
presence of high zooplankton densities, while ingestion of Chironomidae and
Ephemeroptera larvae commenced one day post yolk sac absorption. Ingested
zooplankton was likely primarily composed of Daphnia spp. (Chapter III), which were
about 10 times more abundant in backwater habitats in the Lewis and Clark Delta than in
other habitat types (Chapter IV). During the first week of exogenous feeding, pallid
sturgeon growth was highest when Chironomidae larvae were present in high densities
and in larvae ranging from 20 to 30 and 30 to 40 mm in length growth tended to be
highest when feeding on Ephemeroptera larvae. A composite treatment with lower
densities of each prey type was included in the assessment of the transitional period from
endogenous to exogenous feeding and in the prey taxa-specific growth and survival
experiment, but did not provide the same benefits as treatments with high densities of a
single prey type. Neither did first food uptake occur as early as in the zooplankton
treatment nor did fish grow as well as when offered high densities of Chironomidae
larvae during the first week of exogenous feeding.
Prey selection was assessed in low and high prey density combinations for several
size classes of larval (first feeding larvae to larvae ranging from 30 to 45 mm) and
juvenile pallid sturgeon (70 to 450 mm). Chironomidae larvae were the selected prey type
by all size classes of larval pallid sturgeon. However, in presence of low Chironomidae
larvae densities pallid sturgeon selected positively for Ephemeroptera larvae when
available in high densities. Furthermore zooplankton was frequently incorporated in the
larval pallid sturgeon diet. However not all zooplankton taxa were consumed equally by
pallid sturgeon and ingested zooplankton was primarily composed of Cladocera taxa,
169
primarily Daphnia spp., in all larval size classes. Other zooplankton taxa were rarely
consumed. Juvenile pallid sturgeon ranging from 70 to 200 mm in length selected
positively for Chironomidae larvae and negatively for Ephemeroptera at most prey
density combinations. Similarly juvenile pallid sturgeon ranging from 250 to 450 mm in
length selected positively for Chironomidae larvae and negatively for two types of fish
prey at all prey density combinations.
In the Lewis and Clark Delta, we observed high heterogeneity within habitat types
for many variables and each trophic level and there was no evidence for the general
superiority of one habitat type over another with regard to their suitability as nursery
habitat for age-0 pallid sturgeon. Mean chlorophyll a concentration and macrophyte
density were highest in backwater habitats. Chlorophyll a concentration was positively
correlated with total phosphorus concentration and was inversely correlated with nitrate-
N concentration. Macrophyte density was positively correlated with water depth and
inversely correlated with velocity. The positive correlation with water depth was likely a
habitat type effect as backwater and side channel habitats, which had significant
macrophyte densities, were deeper than Lewis and Clark Lake headwater and main
channel habitats which only had low macrophyte densities or were largely void of
macrophytes. Backwater habitats supported higher zooplankton densities, which could
benefit larval pallid sturgeon for which zooplankton is an appropriate prey resource
(Chapter II and Chapter III), and could also benefit other fishes as most species are
planktivorous during the early life history (Nunn et al. 2012) or even throughout their life
(e.g., paddlefish Polyodon spathula, Wildhaber et al. 2011). Densities of Chironomidae
170
and Caenidae larvae sampled with stovepipe samplers and D-frame nets and densities of
Ephemeridae larvae sampled with stovepipe samplers did not differ between habitat
types. Densities of Ephemeridae larvae sampled with D-frame nets differed between
habitat types and tended to be higher in backwater and side channel habitats.
Furthermore, density of benthic invertebrate taxa that constitute common prey for pallid
sturgeon was highest in backwater habitats. Ephemeroptera larvae, particularly of the
family Caenidae, were the most frequently observed benthic invertebrates, while
Chironomidae larvae were present in lower numbers and other potential prey taxa were
infrequently observed. Caenidae larvae density was negatively correlated with velocity
and positively correlated with macrophyte density for both sampling gears. Ephemeridae
larvae density was positively correlated with chlorophyll α concentration and proportion
of fines in the sediments (i.e., clay and silt). Total benthic invertebrate density was
negatively correlated with velocity and positively correlated with chlorophyll α
concentration for stovepipe samplers and was positively correlated with macrophyte
density for D-frame nets. Pallid sturgeon growth and energy density did not differ among
habitat types and a laboratory reference baseline and final energy densities were similar
to the initial energy density. Furthermore, no habitat differences were observed between
sites that resulted in high growth and low growth. However, sites that fostered high
energy density had significantly lower velocities, finer sediment, higher macrophyte
densities, higher densities of several zooplankton taxa and total zooplankton, and higher
Caenidae larvae and total benthic invertebrate densities. Pallid sturgeon energy density
was positively correlated with Caenidae and Ephemeridae larvae densities, which
suggests that Ephemeroptera larvae constituted an important prey resource. This
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assumption is similar to the results of the laboratory prey selection trials, which suggested
increased consumption of Ephemeroptera larvae when Chironomidae larvae are rare
(Chapter III) as it was the case during the study period in the Lewis and Clark Delta.
However, direct evidence from stomach content analysis was lacking as most prey items
could not be identified due to advanced digestion. Chironomidae larvae were the most
frequently observed prey and could be identified based on head capsules likely due to
their long digestion time (Gannon 1976). Overall our results suggest that conservation
and rehabilitation of low velocity habitats with fine substrate suitable for macrophyte
colonization and enhanced algal production, which foster benthic invertebrate
colonization, may ultimately benefit pallid sturgeon and potentially also a variety of other
fishes in the modified Missouri River ecosystem.
172
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