by tobias rapp - south dakota state university of growth and survival of larval pallid sturgeon: a...

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

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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





selection is indicated by ±, and negative selection is indicated by –. ............................... 81








lower right corner indicate occasional consumption by many individuals. ...................... 82


ranging from 70 to 200 mm at 4 different density combinations of Chironomidae and



by ±, and negative selection is indicated by –. ................................................................. 83

ix


abundance (%) of Chironomidae and Ephemeroptera larvae is plotted against frequency








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


abundance (%) of Chironomidae larvae and fathead minnow is plotted against frequency









x

and Johnny darter. Prey densities are either high or low and are indicated on top for


indicated by –. ................................................................................................................... 87


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







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


abundance (%) of fathead minnow and Johnny darter is plotted against frequency of







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



ANOVA results and χ2-values to Kruskal-Wallis-H test results. Different letters indicate


Table 4-4: Zooplankton densities for habitat types in the Lewis and Clark Delta. Habitat



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


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


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


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


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




SE. Calculated T-values refer to t-test results. Significance was assessed at P < 0.1..... 160



xv




in the Lewis and Clark Delta which supported low and high energy densities of pallid







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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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


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

-0,6

-0,4

-0,2

0,0

0,2

0,4

0,6 High High High

V-I

nd

ex

-0,6

-0,4

-0,2

0,0

0,2

0,4

0,6 High High Low

-0,6

-0,4

-0,2

0,0

0,2

0,4

0,6High Low Low

-0,6

-0,4

-0,2

0,0

0,2

0,4

0,6 LowHigh High

-0,6

-0,4

-0,2

0,0

0,2

0,4

0,6 High HighLow

-0,6

-0,4

-0,2

0,0

0,2

0,4

0,6 Low Low High

-0,6

-0,4

-0,2

0,0

0,2

0,4

0,6 High LowLow

-0,6

-0,4

-0,2

0,0

0,2

0,4

0,6Low

Chironomidae Zooplankton Ephemeroptera

Prey type

Low Low


±±±

_±±

_+ ±

±±±

±_±

±±±

±_±

±±±

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



by ±, and negative selection is indicated by –.

78

0

20

40

60

80

100

Chironomidae: high

Zooplankton: high

Ephemeroptera: highP

rey-s

pec

ific

ab

un

da

nce

(%

)

0

20

40

60

80

100

Chironomidae: high

Zooplankton: high

Ephemeroptera: low

0

20

40

60

80

100

Chironomidae: high

Zooplankton: low

Ephemeroptera: low

0 20 40 60 80 100

0

20

40

60

80

100

Chironomidae: high

Zooplankton: low

Ephemeroptera: high

0

20

40

60

80

100

Chironomidae: low

Zooplankton: high

Ephemeroptera: high

0

20

40

60

80

100

Chironomidae: low

Zooplankton: low

Ephemeroptera: high

0

20

40

60

80

100

Chironomidae: low

Zooplankton: high

Ephemeroptera: low

Frequency of occurence (%)0 20 40 60 80 100

0

20

40

60

80

100

Chironomidae: low

Zooplankton: low

Ephemeroptera: low

Figure 3-2: Food habits of first feeding pallid sturgeon. Prey-specific abundance (%) of

Chironomidae larvae, zooplankton and Ephemeroptera larvae is plotted against frequency






indicate occasional consumption by many individuals.

79

-0,6

-0,4

-0,2

0,0

0,2

0,4

0,6High High High

V-I

nd

ex

-0,6

-0,4

-0,2

0,0

0,2

0,4

0,6 High High Low

-0,6

-0,4

-0,2

0,0

0,2

0,4

0,6 High Low Low

-0,6

-0,4

-0,2

0,0

0,2

0,4

0,6 LowHigh High

-0,6

-0,4

-0,2

0,0

0,2

0,4

0,6High HighLow

-0,6

-0,4

-0,2

0,0

0,2

0,4

0,6 Low Low High

-0,6

-0,4

-0,2

0,0

0,2

0,4

0,6 High LowLow

-0,6

-0,4

-0,2

0,0

0,2

0,4

0,6Low


Prey type

Low Low


±_+

±_+

_+ _

±_±

+_±

+_±

±_+

±±±





selection is indicated by ±, and negative selection is indicated by –.

80

0

20

40

60

80

100

Chironomidae: high

Zooplankton: high


rey-s

pec

ific

ab

un

da

nce

(%

)

0

20

40

60

80

100

Chironomidae: high

Zooplankton: high

Ephemeroptera: low

0

20

40

60

80

100

Chironomidae: high

Zooplankton: low

Ephemeroptera: low

0 20 40 60 80 100

0

20

40

60

80

100

Chironomidae: high

Zooplankton: low

Ephemeroptera: high

0

20

40

60

80

100

Chironomidae: low

Zooplankton: high

Ephemeroptera: high

0

20

40

60

80

100

Chironomidae: low

Zooplankton: low

Ephemeroptera: high

0

20

40

60

80

100

Chironomidae: low

Zooplankton: high

Ephemeroptera: low


0

20

40

60

80

100

Chironomidae: low

Zooplankton: low

Ephemeroptera: low








lower right corner indicate occasional consumption by many individuals.

81

-0,6

-0,4

-0,2

0,0

0,2

0,4

0,6High High High

V-I

nd

ex

-0,6

-0,4

-0,2

0,0

0,2

0,4

0,6High High Low

-0,6

-0,4

-0,2

0,0

0,2

0,4

0,6High Low Low

-0,6

-0,4

-0,2

0,0

0,2

0,4

0,6High Low High


-0,6

-0,4

-0,2

0,0

0,2

0,4

0,6 Low High High

-0,6

-0,4

-0,2

0,0

0,2

0,4

0,6 Low Low High

-0,6

-0,4

-0,2

0,0

0,2

0,4

0,6Low High Low

-0,6

-0,4

-0,2

0,0

0,2

0,4

0,6 Low


Prey type

Low Low





selection is indicated by ±, and negative selection is indicated by –.

82

0

20

40

60

80

100

Chironomidae: high

Zooplankton: high


rey-s

pec

ific

ab

un

dan

ce (

%)

0

20

40

60

80

100

Chironomidae: high

Zooplankton: high

Ephemeroptera: low

0

20

40

60

80

100

Chironomidae: high

Zooplankton: low

Ephemeroptera: low


0

20

40

60

80

100

Chironomidae: high

Zooplankton: low

Ephemeroptera: high

0

20

40

60

80

100

Chironomidae: low

Zooplankton: high

Ephemeroptera: high

0

20

40

60

80

100

Chironomidae: low

Zooplankton: low

Ephemeroptera: high

0

20

40

60

80

100

Chironomidae: low

Zooplankton: high

Ephemeroptera: low

0 20 40 60 80 100

0

20

40

60

80

100

Chironomidae: low

Zooplankton: low

Ephemeroptera: low








lower right corner indicate occasional consumption by many individuals.

83

-0,3

-0,2

-0,1

0,0

0,1

0,2

0,3 High High

-0,3

-0,2

-0,1

0,0

0,1

0,2

0,3

Prey types

High Low

-0,3

-0,2

-0,1

0,0

0,1

0,2

0,3

Chironomidae Ephemeroptera

Prey type

Low High

V-I

nd

ex

-0,3

-0,2

-0,1

0,0

0,1

0,2

0,3

Chironomidae Ephemeroptera

Low Low

+_

+_

±±

+ _


ranging from 70 to 200 mm at 4 different density combinations of Chironomidae and



by ±, and negative selection is indicated by –.

84

Pre

y-s

pec

ific

ab

un

dan

ce (

%)

0

20

40

60

80

100

Chironomidae: high

Ephemeroptera: high

0

20

40

60

80

100

Chironomidae: high

Ephemeroptera: low

Frequency of occurence (%)

0 20 40 60 80 100

0

20

40

60

80

100

Chironomidae: low

Ephemeroptera: low

0 20 40 60 80 100

0

20

40

60

80

100

Chironomidae: low

Ephemeroptera: high


abundance (%) of Chironomidae and Ephemeroptera larvae is plotted against frequency







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

+_

+_

+_

+_



and fathead minnow. Prey densities are either high or low and are indicated on top for


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


0 20 40 60 80 100

0

20

40

60

80

100

Chironomidae: low

Minnow: low


abundance (%) of Chironomidae larvae and fathead minnow is plotted against frequency







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

+_

+_ +

_

+_



and Johnny darter. Prey densities are either high or low and are indicated on top for


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


0 20 40 60 80 100

0

20

40

60

80

100

Chironomidae: low

Johnny darter: low


abundance (%) of Chironomidae larvae and Johnny darter is plotted against frequency of







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

± ±

± ±

± ±

± ±


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


0 20 40 60 80 100

0

20

40

60

80

100

Minnow: low

Johnny darter: low


abundance (%) of fathead minnow and Johnny darter is plotted against frequency of







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

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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

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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

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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

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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).

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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.

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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

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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

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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).

119

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.

120

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

121

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

122

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

123

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

124

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

125

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


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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144

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


(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


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


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


(sediment, %)

2.12 ± 0.43 1.82 ± 0.41 t = 0.359, df = 18, P =

0.72

153



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


(water, mg/L)

2.91 ± 0.20 2.64 ± 0.25 t = 0.797, df = 18, P =

0.44

154



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



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


Z-values refer to Mann-Whitney-U test results. Significance was assessed at P < 0.1.


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


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.


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


(sediment, %)

2.30 ± 0.40 1.35 ± 0.37 t = 1.578, df = 18, P =

0.13

159





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


(water, mg/L)

10.96 ± 0.94 9.47 ± 0.91 t = 0.977, df =18, P =

0.34

160



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






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






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






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).

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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

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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,

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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

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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.

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REFERENCES












by tobias rapp - south dakota state university of growth and survival of larval pallid sturgeon: a...

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