Asian Carp Population Characteristics and Dynamics in the Mississippi River Watershed Christopher Jerod Sullivan Iowa State University

Home , Asian carp, Lake Shetek, Silver carp

Iowa State University Capstones, Theses and Graduate Theses and Dissertations Dissertations

2016 Asian Carp population characteristics and dynamics in the Mississippi River watershed Christopher Jerod Sullivan Iowa State University

Follow this and additional works at: https://lib.dr.iastate.edu/etd Part of the Natural Resources Management and Policy Commons

Recommended Citation Sullivan, Christopher Jerod, "Asian Carp population characteristics and dynamics in the Mississippi River watershed" (2016). Graduate Theses and Dissertations. 16024. https://lib.dr.iastate.edu/etd/16024

This Thesis is brought to you for free and open access by the Iowa State University Capstones, Theses and Dissertations at Iowa State University Digital Repository. It has been accepted for inclusion in Graduate Theses and Dissertations by an authorized administrator of Iowa State University Digital Repository. For more information, please contact [email protected]. Asian Carp population characteristics and dynamics in the Mississippi River watershed

Christopher Jerod Sullivan

A thesis submitted to the graduate faculty in partial fulfillment of the requirements for the degree of MASTER OF SCIENCE

Major: Fisheries Biology

Program of Study Committee: Michael J. Weber, Major Professor Clay L. Pierce Heike Hofmann

TABLE OF CONTENTS

ACKOWLEDGEMENTS ...... iv ABSTRACT ...... 5 CHAPTER 1. GENERAL INTRODUCTION ...... 7 Background ...... 7 Research Needs ...... 11 Goals and Objectives ...... 12 Thesis Organization ...... 12 Literature Cited ...... 13 CHAPTER 2. INTRA-ANNUAL VARIABILITY OF ASIAN CARP POPULATIONS IN THE DES MOINES RIVER, USA ...... 16 Abstract ...... 16 Introduction ...... 17 Materials and Methods ...... 20 Study Area ...... 20 Data Analysis ...... 21 Results ...... 23 Discussion ...... 26 Literature Cited ...... 31 Tables and Figures ...... 36 CHAPTER 3. FACTORS REGULATING YEAR-CLASS STRENGTH OF SILVER CARP THROUGHOUT NORTH AMERICA ...... 41 Abstract ...... 41 Introduction ...... 42 Materials and Methods ...... 45 Study Area ...... 45 Field Sampling ...... 47 Environmental Data ...... 47 Data Analysis ...... 49 Results ...... 51 Discussion ...... 53 Literature Cited ...... 59 Tables and Figures ...... 65 iii

CHAPTER 4. GENERAL CONCLUSIONS ...... 76 Summary ...... 76 Literature Cited ...... 79 APPENDIX A. BIGHEAD CARP ELECTROSHOCKING CATCH-PER-UNIT-EFFORT (CPUE; MEAN ± SE) BY SAMPLING LOCATION AND MONTH DURING 2014 AND 2015 ..... 80 APPENDIX B. BIGHEAD CARP LENGTH-FREQUENCY DISTRIBUTIONS AND PROPORTIONAL SIZE DISTRIBUTION (PSD; P – PREFERRED, M – MEMORABLE, T – TROPHY) INDICES DURING 2014 AND 2015 FROM ELECTROSHOCKING AND TRAMMEL NETS FROM FOUR SITES WITHIN THE DES MOINES RIVER, USA. N = NUMBER OF BIGHEAD CARP CAPTURED AT EACH SITE ...... 81 APPENDIX C. BIGHEAD CARP Wr (MEAN ± SE) BY SAMPLING MONTH COLLECTED AT EDDYVILLE, CLIFFLAND, KEOSAUQUA, AND KEOKUK DURING 2014 AND 2015 ...... 82 APPENDIX D. LEAST SQUARE REGRESSION ANALYSIS AND ASSOCIATED SPEARMAN’S RANK CORRELATION COEFFICIENT (ρ) OBTAINED WHEN REGRESSING RESIDUAL VALUES OBTAINED FOR SILVER CARP POPULATIONS CAPTURED FROM THE UPPER (X AXIS) AND LOWER (Y AXIS) WABASH RIVERS. THE ρ VALUES OBTAINED FROM THIS AND THE OTHER BIVARIATE COMBINATIONS (N = 21) WERE USED TO ASSESS THE SPATIAL EXTENT TO WHICH SILVER CARP SYNCHRONOUSLY RECRUIT ...... 83

ACKOWLEDGEMENTS

First and foremost, I would like to thank Carlos Camacho for all of your help along the duration of the project and being my “mentor”. I could not have imagined being where I am today without your guidance, patience, and your willingness to talk fish with me. More importantly, I couldn’t have asked for a better role model and I am forever in debt to you. I would also like to thank our fantastic suite of technicians who were assigned to the Asian Carp project: Dray Carl, Wes Sleeper, Trevor Blankman, Jed

Seigworth, and Marie Todey. The countless hours in the field colleting fish and in the lab processing samples has made this project possible and I cannot thank you enough. Thank you to the Iowa

Department of Natural Resources (DNR) for funding this project through the Fish and Wildlife Trust

Fund to the Iowa Department of Natural Resources. In addition, I would like to thank Kim Bogenschutz and Jason Euchner of the Iowa DNR for their endless support, guidance, and willingness to collaborate on field work. I have truly enjoyed spending time sampling with you all and talking about anything fish related. I am grateful to Quinton E. Phelps from the Missouri Department of Conservation, David H.

Wahl from the Illinois Natural History Survey, and Robert E. Colombo from Eastern Illinois University for their assistance with Silver Carp collections for my second chapter. I cannot express the gratitude I have towards you all for taking your time to collect and process Silver Carp from multiple sampling locations. I hope that I can repay you all through future collaborations. I would like to thank my advisor,

Michael Weber, for taking me as a master’s student. Thank you for your support and guidance throughout the duration of this project. I truly appreciate your willingness to be flexible and allowing me to operate independently. Thank you to Clay Pierce and Heike Hofmann for serving on my committee and providing valuable guidance and knowledge. I have learned so much from all of you and will carry that knowledge with me in my future endeavors. 5

ABSTRACT

The introduction and spread of invasive species has been considered the most serious and least reversible threat to ecosystem function and native biodiversity. Since their introductions in the 1970s,

Bighead Hypophthalmichthys nobilis and Silver Carp H. molitrix (collectively Asian Carp) have spread throughout the Mississippi River basin and become two of the most recognizable invasive species in

North America. Their migration and possible establishment into reaches of the Upper Mississippi River

(UMR) and its major tributaries is not well understood and knowledge of factors influencing population characteristics and dynamics is needed to facilitate assessment and management. Therefore, the objectives of this study were to evaluate 1) Asian Carp seasonal sampling variation (relative abundance, size structure, and condition) along the Des Moines River in southeastern Iowa and 2) the role of climatic variability in inducing synchronous fluctuations in Silver Carp recruitment in the Missouri, Des Moines,

Mississippi, Illinois, and Wabash rivers. In chapter one of my thesis, Silver Carp populations were collected monthly (April – October) during 2014 and 2015 from four locations in the Des Moines River with boat electroshocking and trammel net sets. Trammel nets rarely captured Silver Carp (mean = 4.9 fish/net ± 1.6 SE; 60% of fish captured in 6.3% of net sets) and therefore were not included in analyses.

Boat electroshocking catch rates (CPUE) exhibited a bimodal distribution with peak CPUEs in late-spring and mid-fall and lower in summer. River discharge was positively related to CPUE at upstream sites but the strength of the correlation decreased at downstream sites. Silver Carp size structure was similar among months and sites except at Cliffland where Silver Carp were smaller during the fall compared to earlier in the year. Finally, Silver Carp condition peaked during late spring and decreased throughout the year with the exception of Carp captured at Keokuk where bimodal peaks occurred during late-spring and early-fall. In chapter two of my thesis, Silver Carp were captured from nine sites across the Mississippi

River watershed during June – September 2015. Silver Carp recruitment was asynchronous (mean ρ = -

0.08 ± 0.13 SE) across the Mississippi River watershed. Populations <300 river km apart were synchronized but populations further apart or in relation to linear distance were asynchronous, suggesting 6

dispersal may be occurring at local scales but local environmental conditions are more important determinants of recruitment at larger scales. Silver Carp recruitment was generally negatively related to variability in river discharge (6 of 9 populations) and positively related to cumulative river discharge during the reproductive season (7 of 9 populations), indicating that extended periods of elevated discharges are important local environmental factors regulating recruitment acting independently among sites. Regionally, Silver Carp recruitment was not significantly related to the North Atlantic Oscillation

Index (NAO), El Niño Southern Oscillation Index (ENSO), or Palmer Hydrological Drought Index

(PHDI), indicating that local environmental factors have more influence on Silver Carp year-class strength than broad climatic conditions. Collectively, these findings suggest that Silver Carp standardized sampling efforts should be concentrated during May-June or September-October when localized Silver

Carp catch rates are highest and vulnerable to boat electroshocking. In addition, Silver Carp exhibit asynchronous fluctuations in recruitment and prevailing local environmental conditions regulate Carp year-class strength. As such, sampling efforts targeting Silver Carp populations during the spring may be beneficial as local abundances are highest and the removal of potential spawning stock biomass could aid in decreasing annual reproductive outputs, especially during years where environmental conditions are conducive to local reproductive success (i.e., sustained above average discharge rates). Collectively, understanding spatiotemporal fluctuations in Asian Carp dynamic rates will aid managers in determining how populations will respond to both local and regional environmental conditions, improving our understanding of a highly invasive and injurious fish species.

CHAPTER 1. GENERAL INTRODUCTION

Background

Biological invasions resulting from human activities are commonplace in recent history (Pimm et al. 1995; Levine and D’Antonio 2003; Hulme 2009), homogenizing local fauna and flora (Lodge 1993;

Lockwood and McKinney 2001). This spread, and subsequent impacts, of nonnative species is perhaps one of the most serious (Mooney and Hobbs 2000; Carlton 2001) and least reversible (Kolar and Lodge

2002) human-induced changes occurring around the world. When invaders become established, their effects on ecosystems are wide ranging from negligible (e.g., Pumpkinseed Lepomis gibbosus; Moyle

1976) to severe (e.g., Common Carp Cyprinus carpio; Weber and Brown 2009). Globally, over one thousand different species (terrestrial and aquatic) have been transferred among countries, but the exact number of introductions is likely conservative due to a large number that go undetected for long periods of time (Kolar and Lodge 2002). In aquatic systems around the world, biological invasions are increasing in frequency at an alarming rate (e.g., Ruiz et al. 1999). In the United States alone, 245 fishes have been introduced since the 1800s, resulting in 122 species successfully establishing populations (NAS 2016).

Species are introduced through a variety of pathways, including intentionally for commercial (e.g.,

Common Carp; Weber and Brown 2009) and recreational purposes (e.g., Smallmouth Bass Micropterus dolomieu in north temperate lakes; Vander Zanden et al. 2004) or accidentally through removal of environmental barriers which creates a corridor for invader passage between previously unconnected systems (e.g., Sea Lamprey Petromyzon marinus and Zebra Mussels Dreissena polymorpha; Dymond

1922; Hebert et al. 1989).

Recently, the invasion of Asian Carp Hypophthalmichthys spp. throughout the Mississippi River basin has been well publicized and elicited substantial concern among ecologists. Asian Carp are native to eastern Asia, ranging from Russia to northern Vietnam (Fuller et al. 1999; Kolar et al. 2007). Both species have been widely introduced throughout the world both intentionally for consumption and 8

biomanipulation purposes and unintentionally through escapement and range expansion in various system types (e.g., reservoirs, lakes, rivers, ponds; see Kolar et al. 2007). Asian Carp were originally introduced into private fish culture ponds in Arkansas, USA in 1973 to reduce algal blooms and improve water quality (Freeze and Henderson 1982). However, Asian Carp escaped and invaded tributaries of the

Mississippi River during floods in the mid-1970s. By 1981, several individuals were captured from

Crooked Creek in northeastern Arkansas (Freeze and Henderson 1982), representing range expansion in a relatively short period. Since their escape into Arkansas rivers, Asian Carp have migrated upstream in the

Mississippi River and associated tributaries. As of 2016, Asian Carp have been captured in the Missouri

(Schrank et al. 2001; Schrank and Guy 2002; Papoulias et al. 2006; Wanner and Klumb 2009; Wanner and Klumb 2009; Deters et al. 2013; Hayer et al. 2014), Illinois (DeGrandchamp et al. 2007; Irons et al.

2007; Lamer et al. 2010; Sass et al. 2010), Ohio (NAS 2016), Wabash (Stuck 2010), and upper

(Lohmeyer and Garvey 2010; Tripp and Garvey 2010), middle (Williamson and Garvey 2005), and lower

(Varble et al. 2007) Mississippi rivers.

Asian Carp are able to occupy and establish populations in a wide array of habitats due to their wide range of environmental tolerances (e.g., temperature, turbidity, water quality) and life history characteristics (e.g., rapid growth, early maturation, high fecundity, broad diets). Asian Carp reproduction has been documented in pool 20 of the upper Mississippi River (UMR) downstream of Lock and Dam 19, indicating these fish have become successfully established (i.e., Lohmeyer and Garvey

2009; NAS 2016). Asian Carp have rapid growth (>550 mm by age-3), early maturation (2-3 years of age; Schrank and Guy 2002; Williamson and Garvey 2005), high fecundity (>100,000 eggs/female;

Garvey et al. 2006), and protracted spawning (Schrank and Guy 2002). These characteristics allow Asian

Carp, and other successful invaders, to attain high densities (5.5. metric tons/river km; Sass et al. 2008) and negatively alter aquatic environments. Coupled with their abilities to establish populations in a relatively short amount of time, Asian Carp can migrate more than 3 km daily, with maximum observed total movement >400 km over two years (DeGrandchamp et al. 2008). Asian Carp more frequently move 9

upstream, as much as 130 km, and movements tend to increase during the spring with rises in temperature and flow (DeGrandchamp et al. 2008; Coulter et al. 2016), greatly expanding their potential range within the UMR. Due to their migration capabilities within the UMR, contrasting levels of population densities exist, especially for newly invaded river reaches. For example, Silver Carp catches have typically composed >50% of the fish collected on the La Grange reach of the Illinois River since 2008 (first detected in 1998; Sass et al. 2010), whereas Silver Carp in South Dakota tributaries of the upper Missouri

River composed >50% of catches beginning in 2012 (first detected in 2005; Hayer et al. 2014). In addition, invasive Carp may be able to persist in areas where reproduction is insufficient through dispersal from areas where populations are established (source-sink dynamics; Pulliam 1988). As a result, robust monitoring protocols that identify population status and trends of Asian Carp on various invasion fronts is necessary.

Natural resource agencies recognize the importance of collecting basic Asian Carp population information and its value in monitoring the spread and management of these populations (Conover and

Simmonds 2007). In addition, population characteristics (condition, size structure, abundance) provide insights to their current status, habitat quality of inhabited systems, and their influence on population structure. Besides inferences about population structure, information on Asian Carp population characteristics in the upper Mississippi River watershed could be compared to populations inhabiting tributaries across their range, informing managers on local population structures and potential abiotic and biotic conditions. Thus, most state and federal natural resource agencies throughout the range of invasive

Asian Carp monitor populations on a regular basis. Yet, current sampling occurs at various times of the year. For a variety of species, seasonal sampling variation has been documented and can influence interpretation of population structure. Generally, population surveys reported higher catches during the spring and fall (Pope and Willis 1996) in response to environmental conditions compared to other times of the year (i.e., summer). For example, Smallmouth Bass Micropterus dolomieu in eastern South Dakota lakes exhibit a high degree of temporal variation in population structure, potentially due to the seasonal 10

movement of adult fish and recruitment of young-of-the-year fish to sampling gear (Bacula et al. 2011).

In contrast, there is a lack of information regarding the spatiotemporal variability of environmental variables and associated variation in Asian Carp distribution locally and regionally. Southeastern Iowa tributaries of the Mississippi River offer a unique opportunity to study temporal variation in Asian Carp population characteristics along an invasion edge. Asian Carp densities are higher in the Mississippi

River and tributaries below Lock and Dam 19 (LD19) compared to populations located upstream above

LD19 (NAS 2016). By evaluating temporal variation in Asian Carp populations, population trends (i.e., intra-annual fluctuations in abundance) can be revealed which can provide insight that will aid in improving capture and subsequent management efforts along the leading edge of the invasion front.

Given that Asian Carp are mobile species and mechanistic processes such as source-sink dynamics are thought to regulate populations, fish dispersal from downstream to upstream habitats has the ability to synchronize population dynamics. In contrast, large-scale spatial synchrony is now considered a common ecological phenomenon (Ranta et al. 1998) where population dynamics may fluctuate synchronously at regional scales as a result of similarities in broad-scale environmental conditions regulating populations (i.e., Moran effect; Moran 1953). Partitioning the roles of dispersal from environmental perturbations in synchronizing population fluctuations can alter the understanding of dynamic rates of spatially distinct populations. Numerous studies focus on spatial patterns in fish recruitment across local-scales, with populations fluctuating inter-annually due to localized biotic or abiotic conditions (e.g., Grenouillet et al. 2001; Penha et al. 2014). For example, Bighead Carp (similar reproductive requirement’s as Silver Carp; see Kolar et al. 2007) in two separate reaches of the Missouri

River were shown to exhibit dissimilar populations dynamic rates attributed to localized environmental conditions (Wanner and Klumb 2009). In South Dakota tributaries, local-scale similarities and fluctuations in dynamics rates were hypothesized to be augmented through dispersal while regional-scale differences in dynamics rates between populations were attributed to density dependent mechanisms

(Hayer et al. 2014). Conversely, fluctuations in population dynamics may be attributed to environmental 11

conditions rather than density-dependent interactions. Similar to dispersal, large-scale, stochastic, climatic perturbations can induce synchronous fluctuations of dynamic rates on a varying, but larger scale

(Meyer et al. 1997; Phelps et al. 2008; Dembkowski et al. 2016; Honsey et al. 2016) rather than a local- scale where dispersal can fluctuate dynamic rates. For example, erratic, but synchronous, fluctuations in

Common Carp recruitment in Glacial Lakes produced populations dominated by few age-classes as a result of similarities in water temperature, precipitation and wind (Phelps et al. 2008). Similarly, Asian

Carp populations have been documented to have erratic recruitment, composed of only a few year-classes.

For example, Silver Carp age structure in South Dakota was dominated by the 2010 year-class, coinciding with high river discharge occurring that year in portions of the Missouri River (Hayer et al. 2014).

Similarly, Bighead Carp populations in the lower Missouri River were dominated by the 1993 and 1994 year-classes (Schrank and Guy 2002) which coincided with major flooding in the Missouri River. Other studies have also documented rises in river discharge (e.g., flood) during periods above 17°C coinciding with successful Silver Carp reproduction in the UMR (Garvey et al. 2006; DeGrandchamp et al. 2007;

Lohmeyer and Garvey 2009). Collectively, such studies indicate that Asian Carp year-class strength may be influenced by large-scale climatic effects. Understanding fluctuations in dynamic rates and the large- scale climatic perturbations that influence them is critical for understanding underlying mechanisms influencing recruitment and subsequent adult abundance.

Research Needs

There is a paucity of knowledge associated with established and migrating Asian Carp populations that is critical to understanding patterns of population fluctuations on a local and regional scale. To effectively monitor large-scale range expansion of these species, knowledge of temporal variation in population characteristics as well as critical environmental variables influencing capture is needed. In doing so, the information provided will be a crucial step in understanding dispersal, and possible establishment, characteristics of Asian Carp into higher reaches of the UMR. Additionally, the degree of Asian Carp recruitment synchrony among the Mississippi River watershed as well as the 12

influence of climate and dispersal on recruitment may further our knowledge of a highly invasive species reproductive habits. Such information will aid in our understanding of local and regional mechanistic processes influencing dynamic rates, manipulating management scales for Asian Carp. Collectively, the information gained from this project will provide valuable insights of the life history characteristics of an invasive species on the invasion front in the UMR and will help guide future managers conservation efforts at local and regional scales.

Goals and Objectives

The overall goal of this project was to improve current monitoring protocols and understanding of processes regulating Asian Carp recruitment within the Mississippi River watershed. The specific objectives of this project were as follows:

1) Evaluate temporal (i.e., seasonal and annual) trends in Asian Carp population characteristics

(abundance, size structure, condition) within a major southeastern Iowa tributary.

2) Evaluate patterns of Silver Carp recruitment synchrony throughout the Mississippi River

watershed.

Thesis Organization

Chapter 1 provides a general introduction to the thesis. Chapters 2 and 3 address the research objectives outlined above: Chapter 2 describes intra-annual trends in Asian Carp populations along the

Des Moines River, USA and Chapter 3 describes the factors regulating year-class strength of Silver Carp throughout North America. Chapter 4 summarizes the general conclusions of the thesis.

Literature Cited

Bacula TD, Blackwell BG, Willis DW (2011) Seasonal sampling dynamics of Smallmouth Bass (Micropterus dolomieu) in northeastern South Dakota. Journal of Freshwater Ecology 26:345-356 Cartlon JT (2001) Introduced species in U.S. coastal waters: environmental impacts and management priorities. Pew Oceans Commission, Arlington, VA. 35pp Conover GC, Simmonds R, Whalen M (2007) Management and control plan for Bighead, Black, Grass, and Silver carps in the United States. Asian Carp Working Group, Aquatic Nuisance species Task Force, Washington, D.C. pp 71 Coulter AA, Bailey EJ, Keller D, Goforth RR (2016) Invasive Silver Carp movement patterns in the predominantly free-flowing Wabash River (Indiana, USA). Biological Invasions 18:471-485

DeGrandchamp KL, Garvey JE, Csoboth LA (2007) Linking adult reproduction and larval density of invasive Carp in a large river. Transactions of the American Fisheries Society 136:1327-1334 Dembkowski DJ, Willis DW, Wuellner MR (2016) Synchrony in larval Yellow Perch abundance: the influence of the Moran Effect during early life history. Canadian Journal of Fisheries and Aquatic Sciences. DOI: 10.1139/cjfas-2015-0310 Deters JE, Chapman DC, McElroy B (2013) Location and timing of Asian Carp spawning in the lower Missouri River. Environmental Biology of Fishes 96:617-629 Dymond JR (1922) A provisional list of the fishes of Lake Erie. University of Toronto Studies. Publications of the Ontario Fisheries Research Laboratory 4:57-73 Freeze M, Henderson S (1982) Distribution and status of the Bighead Carp and Silver Carp in Arkansas. North American Journal of Fisheries Management 2:197-200 Fuller PL, Nico LG, Williams JD (1999) Nonindigenous fishes introduced into inland waters of the United States. American Fisheries Society, Special Publication 27, Bethesda. 613 pp Grenouillet G, Hugueny B, Carrel GA, Olivier JM, Pont D (2001) Large-scale synchrony and inter-annual variability in Roach recruitment in the Rhone River: the relative role of climate factors and density-dependent processes. Freshwater Biology 46:11-26 Hayer CA, Breeggemann JJ, Klumb RA, Graeb BD, Bertrand KN (2014) Population characteristics of Bighead and Silver carp on the northwestern front of their North American invasion. Aquatic Invasions 9(3): 289-303 Hebert PD, Muncaster BW, Mackie GL (1989) Ecological and genetic studies on Dreissena polymorpha (Palla): a new mollusc in the Great Lakes. Canadian Journal of Fisheries and Aquatic Sciences 46:1587-1591 Honsey AE, Brunnel DB, Troy CD, Fielder DG, Thomas MV, Knight CT, Chong SC, Höök TO (2016) Recruitment synchrony of Yellow Perch (Perca flavescens, Percidae) in the Great Lakes regions, 1966-2008. Fisheries Research 181:214-221 Hulme PE (2009) Trade, transport and trouble: managing invasive species pathways in an era of globalization. Journal of Applied Ecology 46:10-18 Irons KS, Sass GG, McClelland MA, Stafford JD (2007) Reduced condition factor of two native fish species coincident with invasion of nonnative Asian Carps in the Illinois River, U.S.A. Is this evidence for competition and reduced fitness? Journal of Fish Biology 71:258-273 14

Kolar CS, Lodge DM (2002) Ecological predictions and risk assessment for alien species. Science 298:1233-1236 Kolar CS, Chapman DC, Courtenay WR, Housel CM, Williams JD, Jennings DP (2007) Bigheaded Carps: a biological synopsis and environmental risk assessment. Special Publication 33. American Fisheries Society, Bethesda, Maryland Lamer JT, Dolan CR, Petersen JL, Chick JH, Epifanio JM (2010) Introgressive hybridization between Bighead Carp and Silver Carp in the Mississippi and Illinois rivers. North American Journal of Fisheries Management 30:1452-1461 Levine JM, D’Antonio CM (2003) Forecasting biological invasions with increasing international trade. Conservation Biology 17:322-326 Lockwood JL, McKinney ML (2001) Biotic homogenization. Dordrecht, The Netherlands: Kluwer Lodge DM (1993) Biological invasions: lessons for ecology. Trends in Ecology and Evolution 8:133-137 Lohmeyer AM, Garvey JE (2009) Placing the North American invasion of Asian Carp in a spatially explicit context. Biological Invasions 11:905-916 Mooney HA, RJ Hobbs (2000) Invasive species in a changing world: Washington D.C., Island Press 457 Moran PA (1953) The statistical analysis of the Canadian Lynx cycle, II. Synchronization and Meteorology. Australian Journal of Zoology 1:291-298 Moyle PB (1976) Inland fishes of California. University of California Press, Berkeley, CA NAS (2016) Hypophthalmichthys nobilis (Bighead Carp). Nonindigenous Aquatic Species. http://nas2.er.usgs.gov/viewer/omap.aspx?SpeciesID=551 Papoulias DM, Chapman D, Tillitt DE (2006) Reproductive condition and occurrence of intersex in Bighead and Silver carp in the Missouri River. Hydrobiologia 571:355-360 Penha J, Mateus L, Lobón-Cerviá J (2014) Population regulation in a Neotropical seasonal wetland fish. Environmental Biology of Fishes. DOI: 10.1007/s10641-014-0336-6 Pimm SL, Russel GJ, Gittleman JL, Brooks TM (1995) The future of biodiversity. Science 269:347-349 Pope KL, Willis DW (1996) Seasonal influences on freshwater fisheries sampling data. Reviews in Fisheries Science 4:57-73 Pulliam HR (1988) Sources, sinks, and population regulation. The American Naturalist 132:652-661 Ranta E, Kaitala V, Lindström J (1998) Spatial dynamics of populations: In: Modeling Spatiotemporal Dynamics in Ecology. Eds. J Bascompte and R.V. Solé, Springer, Berlin. 47-62pp Ruiz GM, Fofonoff P, Hines AH, Grosholz ED (1999) Non-indigenous species as stressors in estuarine and marine communities: assessing invasion impacts and interactions. Limnology and Oceanography 44:950-972 Sass GG, Cook TR, Irons KS, McClelland MA, Michaels NN, O’Hara TM, Stroud MR (2010) A mark- recapture population estimate for invasive Silver Carp (Hypophthalmichthys molitrix) in the La Grange Reach, Illinois River. Biological Invasions 12:433-436 Schrank SJ, Braaten PJ, Guy CS (2001) Spatiotemporal variation in density of larval Bighead Carp in the lower Missouri River. Transactions of the American Fisheries Society 130:809-814 15

Schrank SJ, Guy CS (2002) Age, growth, and gonadal characteristics of adult Bighead Carp, Hypophthalmichthys nobilis, in the lower Missouri River. Environmental Biology of Fishes 64:443-450 Stuck JG (2012) Comparison of Silver Carp population demographics in an impounded and a free flowing river. Masters Thesis. Eastern Illinois University. Available: http://thekeep.eiu.edu/theses/1046 Tripp S, Garvey JE (2011) Fish passage in the upper Mississippi River system. Fisheries and Illinois Aquaculture Center Department of Zoology Southern Illinois University, Annual report Vander Zanden MJ, Olden JD, Thorne JH, Mandrak NE (2004) Predicting occurrences and impacts of Smallmouth Bass introductions in north temperate lakes. Ecological Applications 14:132-148 Varble KA, Hoover JJ, George SG, Murphy CE, Killgore KJ (2007) Floodplain wetlands as nurseries for Silver Carp, Hypophthalmichthys molitrix: A conceptual model for use in managing local populations. ANSRP Technical Notes Collection (ERDC/TN ANSRP-07-4), Vicksburg, Mississippi Wanner GA, Klumb RA (2009) Asian Carp in the Missouri River: Analysis from multiple Missouri River habitat and fisheries programs. National Invasive Species Council materials. Paper 10 National Invasive Species Council materials. Paper 10 Wanner GA, Klumb RA (2009) Length-weight relationships for three Asian Carp species in the Missouri River. Journal of Freshwater Ecology 24:489-495 Weber MJ, Brown ML (2009) Effects of Common Carp on aquatic ecosystems 80 years after “carp as a dominant”: ecological insights for fisheries management. Reviews in Fisheries Science 17:270- 278 Williamson CJ, Garvey JE (2005) Growth, fecundity, and diets of newly established Silver Carp in the middle Mississippi River. Transactions of the American Fisheries Society 134:1423-1430

CHAPTER 2. INTRA-ANNUAL VARIABILITY OF ASIAN CARP POPULATIONS IN THE DES

MOINES RIVER, USA

Abstract

Since their introduction in the 1970s, Asian Carp Hypophthalmichthys spp. have spread throughout the Mississippi River basin (MRB). Management of any species relies on an accurate understanding of population characteristics and dynamics. However, Asian Carp seasonal sampling variation is unknown. Sampling during periods of peak catch rates would facilitate Asian Carp assessment and management, improving monitoring and removal techniques. My objective was to evaluate Asian Carp seasonal sampling variation with boat electroshocking and trammel nets. Asian Carp were collected monthly (April – October) during 2014 and 2015 from four locations in the Des Moines

River, Iowa, USA. Trammel nets rarely captured Silver Carp (mean = 4.9 fish/net ± 1.6 SE; 60% of fish captured in 6.3% of net sets) and therefore were not included in analyses. Electroshocking catch rates

(CPUE) exhibited a bimodal distribution, with peak CPUE in late-spring and mid-fall and lower in summer during periods of high water temperature. Catch rates were positively related to river discharge at upstream sites but the strength of the correlation decreased at downstream sites. Silver Carp size structure was similar among months and sites except Silver Carp captured at Cliffland were smaller during the fall compared to earlier in the year. Finally, Silver Carp condition peaked during late spring and decreased throughout the year except condition of Carp captured at Keokuk where peaks were observed during both late-spring and early-fall. My results suggest that sampling of Silver Carp using electroshocking in late-spring (May-June) and fall (September-October) results in higher catch rates compared to summer sampling and a more representative size structure. Thus, monitoring and surveillance programs should establish standardized sampling programs during these periods of high vulnerability and densities in order to manage the spread and impacts of Silver Carp at state- and region- wide scales.

Introduction

The spread and subsequent impacts of nonnative species introductions is perhaps one of the most serious (Mooney and Hobbs 2000; Carlton 2001) and least reversible (Kolar and Lodge 2002) human- induced changes occurring around the world. Recently, the invasion of Silver Hypophthalmichthys molitrix and Bighead H. nobilis carp throughout the Mississippi River basin has been well-publicized and elicited substantial concern among scientists and the general public. Since their escape into central

Arkansas rivers during the mid-1970s, Asian Carp have migrated upstream throughout the Mississippi

River basin. As of 2016, Asian Carp have been captured in the Missouri (Papoulias et al. 2006; Wanner and Klumb 2009a; Deters et al. 2013), Illinois (DeGrandchamp et al. 2007; Irons et al. 2007; Lamer et al.

2010; Sass et al. 2010), Ohio (NAS 2016), Wabash (Coulter et al. 2015: Stuck et al. 2015), and upper

(Lohmeyer and Garvey 2010; Tripp and Garvey 2010), middle (Williamson and Garvey 2005), and lower

(NAS 2016) Mississippi River watershed. Once present, relative abundance of Asian Carp can increase dramatically. For example, Silver Carp electroshocking catch-per-unit-effort (CPUE) increased from zero to nearly 36 fish per hour (max CPUE = 76 fish per hour) in the Big Sioux, James, and Vermillion rivers in southeast South Dakota over a four year period (Hayer et al. 2014b). As a result, robust monitoring protocols that identify Asian Carp abundance status and trends are necessary for documenting initial introductions and subsequent fluctuations in abundance.

Currently, there is a lack of standardized sampling methodology to capture, monitor, and manage invasive Asian Carp. Standardized sampling is a critical component of fisheries management (Bonar et al. 2009). Across species and systems, standardized sampling programs provide supporting information needed throughout the decision making process as well as providing a framework for developing alternatives to current management programs (Gablehouse et al. 1992; Bonar and Hubert 2002). These standardized collections are oftentimes developed using documented trends in populations to avoid variation in populations, to be simple, and to be cost effective (Bonar and Hubert 2002). In contrast, laborious species collections lacking standardized methodologies are often difficult (e.g., time/labor 18

constraints or erratic species capture) and can hinder a managers’ ability to interpret a species’ current population status. Further, subsequent comparisons among populations throughout their range can be misleading, potentially influencing subsequent management actions. As such, standardization of fish sampling can provide clear benefits, especially in the case of an invasive fish species such as Asian Carp.

Although the efficiency of various gears used to assess Asian Carp populations has recently received considerable attention (e.g., daytime electroshocking, mini-fyke nets, hoop netting, gill netting, pound nets, etc.; Koel et al. 2000; Irons et al. 2007; McClelland and Sass 2008; Wanner and Klumb

2009a; Collins et al. 2015), the extent that seasonality and environmental characteristics affects capture rates has yet to be evaluated. Identifying seasonal sampling variation is important because capture rates and size structure of fishes captured in sampling gears can vary temporally due to movement patterns

(Miller and Scarnecchia 2008; Béguer-Pon et al. 2015), spawning migrations (Herbst et al. 2015), local environmental conditions (Cowley et al. 2007; Jones and Stuart 2009; Muhlfeld et al. 2012; Gardner et al.

2013), prey availability (Bowlby and Hoyle 2011), and the annual flux of young-of-year fish recruiting to sampling gears (Bacula et al. 2011; Neal and Prchalová 2012). In lakes, seasonal sampling variation has been attributed to surface water temperatures (e.g., Bacula et al. 2011) and spawning activity (e.g., Lott

2000; McKibbin 2002; Herbst et al. 2015). In contrast, seasonal sampling variation in rivers is more complex due to the aforementioned variables (Miller and Scarnecchia 2008; Zimmer et al. 2010;

Muhlfeld et al. 2012; Gardner et al. 2013) in addition to variable river flow (Cowley et al. 2007) and temporary floodplain connectivity (Jones and Stuart 2008), potentially influencing fisheries sampling success.

Seasonal sampling variation has been documented for various freshwater fishes, with higher catches generally reported during the spring and fall in response to environmental conditions (Pope and

Willis 1996). Substantial research has been devoted to documenting Asian Carp expansion and subsequent increases in densities (e.g., Irons et al. 2007; Hayer et al. 2014a). However, information regarding Asian Carp seasonal sampling variation in relation to environmental conditions is lacking.

Asian Carp spawning varies as a function of both surface water temperature and river flow rates. Asian 19

Carp typically spawn in rapidly flowing river segments (thalweg habitats; 0.6-2.3 m/s) in conjunction with temperatures ranging from 18-30°C (Chang 1966; Verigin et al. 1978; Kaul and Rishi 1993), with sudden increases in river flow serving as a primary driver of spawning (Zhang et al. 2000; Li et al. 2006;

Wang et al. 2008). Within Mississippi River tributaries, Asian Carp movements increase during the spring and early summer when fish generally migrate upstream in response to increasing river flow and water temperatures (Degrandchamp et al. 2008; Coulter et al. 2016). Additionally, Asian Carp can migrate more than 3 km daily (>400 km over two years; DeGrandchamp et al. 2008) while frequently moving upstream (Calkins et al. 2012). Combined, spatiotemporal variability of environmental variables and associated Asian Carp behavior (i.e., timing and extent of spawning movements) has the ability to alter Asian Carp distribution locally and regionally, potentially influencing population indices (i.e., relative abundance, size structure, and condition) and perception of population status.

Monitoring population characteristics of invasive fishes can provide valuable insights to the cumulative interactions of dynamic rates (i.e., recruitment, growth, and mortality) and their influence on population structure. Natural resource agencies recognize the importance and necessity of collecting basic Asian Carp population information and its value in monitoring the spread and management of these populations (Sakai et al. 2001; Conover and Simmonds 2007). Yet, Asian Carp standardized sampling protocols have yet to be developed. Therefore, the objective of my study was to evaluate potential temporal variation in Asian Carp catch rates, size structure, and relative weight using electroshocking and trammel nets. I hypothesized that catch rates of Asian Carp would be highest during the spring and fall months, size structure of Asian Carp would vary seasonally due to adult movement patterns, and relative weight of Asian Carp will be highest during the spring in response to spring spawning activity (Kolar et al. 2007).

Materials and Methods

Study Area

The Des Moines River originates in Lake Shetek, Minnesota and flows 845 km to the confluence of the Mississippi River at Keokuk, Iowa. The Des Moines River drains an area of 40,940 km2 with a mean daily discharge of 232 m3/sec (USGS 2013). An array of anthropocentric alterations have been completed along the river including dams, levees, and submerged weirs. The river is channelized and subjected to rapidly changing hydrographs. Specifically, the Des Moines River contains the Ottumwa

(near Ottumwa, Iowa), Red Rock (near Pella, Iowa), and Saylorville (near Des Moines, Iowa) dams, which mitigate flood damage in adjacent cities. Additionally, Lock and Dam 19 (LD 19; Keokuk, Iowa) is approximately six river kilometers upstream from the Des Moines and Mississippi river confluence, which restricts fish movement upriver (Tripp et al. 2013).

Field Sampling

Asian Carp were sampled once monthly from April to October 2014 and 2015 at four sites in the

Des Moines River (Figure 1) using daytime boat electroshocking and stationary trammel nets. Asian

Carp are difficult to capture (Williamson and Garvey 2005) and have been sampled with variable success using a variety of gears (Koel et al. 2000; Hayer et al. 2014b; Collins et al. 2015). However, a wide array of Asian Carp sizes appear to be effectively captured using boat electroshocking (e.g., McClelland and

Sass 2008; Sass et al. 2010; Stuck et al. 2015) whereas larger Asian Carp are more commonly captured using passive gears (e.g., trammel nets; Wanner and Klumb 2009a). Therefore, trammel net sets in conjunction with boat electroshocking were both used and compared for their ability to sample Asian

Carp. Daytime boat electroshocking (DC; 4-13 amps, 100-500 V, 60 pulses per second with two netters) transects were 15 min in duration with three transects conducted at each site. Electroshocking was conducted parallel to the shoreline, targeting channel border and backwater habitats less than 4 m deep

(DeGrandchamp et al. 2008). When river conditions allowed, stationary trammel nets (100 m long, 10- cm-bar inner mesh) were fished in areas of low flow (e.g., eddies, dike pools, inside river bends, etc.) less 21

than 2 m deep. One end of the trammel net was anchored on shore and the remaining net was stretched towards deeper water or an opposite shore, restricting Carp movement out of backwater areas. Both gears were fished simultaneously by setting a trammel net first to block Asian Carp escapement from backwater areas then electroshocking. All Asian Carp captured were sexed (male, female, immature, or unknown), weighed (kg), and measured (mm; total length [TL]). Thalweg water temperature (Yellow Springs

Instruments 550A; Celsius) and conductivity (EC400 ExStik 2 Conductivity Meter) were measured monthly during fish sampling at each site. Additionally, mean daily discharge values (cubic meters per second [m3/s]) were obtained from U.S. Geological Survey gaging stations upstream from each sampling location present at Tracy (gaging station number #05488500 ), Ottumwa (#05489500), and Keosauqua

(#05490500), Iowa.

Data Analysis

Asian Carp relative abundance was indexed as catch-per-unit-effort (CPUE) for daytime boat electroshocking or trammel netting by month. Trammel net CPUE was calculated as the number of fish captured per net lift, whereas electroshocking CPUE was calculated as number of fish collected per hour of electroshocking. Asian Carp CPUE data were zero-inflated (e.g., temporary absence or lack of Asian

Carp capture) and over-dispersed. Thus, a negative binomial generalized linear model was used to assess differences in monthly mean CPUE of Asian Carp across sites. Modeling using a negative binomial distribution is useful when data are counts, in particular small counts, as well as when the mean and variance are correlated (Gardner et al. 1995). The data were modeled as count for a given amount of effort:

푦푖푗푘푙~푁푒푔푎푡푖푣푒 퐵푖푛표푚푖푎푙(휆푖푗푙 ∗ 휑푖푗푘푙)

where i denotes the month, j is the location, k is the individual net or electroshocking run, and l is the year. In equation 1, λijl is the CPUE for month i, location j, and year l while φijkl is the effort (offset) for year l, month i, location j, and net k. Pairwise comparisons of monthly CPUE rate ratios (proportional 22

changes between months) were used to compare CPUE rates among months within each sampling location. A post hoc Tukey HSD test using Bonferroni corrected P-values was used to determine which year, sites, and months differed.

The influence of mean daily discharge, water temperature, and conductivity on Asian Carp capture rates were evaluated using Pearson correlations coefficients. Due to the absence of a U.S.

Geological Survey gauging station upstream from Keokuk, Iowa, mean daily discharge values obtained from the gaging station at Keosauqua (80.0 river miles upstream) were used to evaluate the relationship of mean daily discharge and capture rates of Asian Carp at Keokuk. For each site and variable, a randomization test for significance involving 5000 iterations was used to compare a generated distribution of the calculated Pearson correlation coefficient values. In order to compute a P-value (α = 0.05), the number of generated Pearson correlation coefficient values greater than the Pearson correlation coefficient value obtained from the original data was divided by the number of iterations (5000).

Bonferroni corrected P-values were used to determine significant relationships.

Asian Carp total length data were grouped by month and length groups (stock 250 – 449.9 mm; quality 450 – 559.9 mm; preferred 560 – 739.9 mm; memorable 740 – 929.9 mm; trophy ≥ 930 mm;

Phelps and Willis 2013). A chi-square test for differences in probabilities was used to assess differences in Asian Carp length-group frequencies among months. If a difference was detected, individual chi- square tests were used to determine differences between months.

Body condition was indexed as relative weight (Wr) using standard weight (Ws; J. Lamer,

Western Illinois University, unpublished data) averaged by length groups (stock 250 – 449.9 mm; quality

450 – 559.9 mm; preferred 560 – 739.9 mm; memorable 740 – 929.9 mm; trophy ≥ 930 mm; Phelps and

Willis 2013). Length categories with fewer than five fish captured on a specific sampling date were excluded from Wr calculations. A repeated measures analysis of variance (ANOVA) was used to test for length group, site, month, and year differences in Wr. If significant differences were detected, pairwise t- tests using Bonferroni corrected P-values were used to determine which groups differed. All statistical analyses were conducted in Program R Software Version 3.2.0 with a significance level of α = 0.05. 23

Results

Only 66 Bighead Carp were captured during 2014 and 2015, making temporal population characteristics difficult to interpret due to small sample sizes. Due to few captures overall, Bighead Carp information (i.e., catch rates, size structure, and condition) was excluded from analyses. In all, electrofishing captured a total of 37 Bighead Carp while trammel nets captured a total of 29 Bighead

Carp. Bighead Carp electroshocking capture rates exhibited a less predictable pattern compared to Silver

Carp, as catch rates exhibited a bimodal distribution in 2014 and a more erratic pattern in 2015 where catches peaked during late spring (Appendix A). At Cliffland and Keokuk, Bighead Carp catch rates peaked during October while catch rates at Keosauqua peaked during May and September (Appendix A).

During 2015, Bighead Carp were captured more frequently and catch rates were highest during late spring for all sites except Eddyville where catch rates peaked in the fall (Appendix A).

Bighead Carp size structure varied spatially in the Des Moines River (Appendix B). Bighead

Carp at downstream sites ranged from 397 mm to 998 mm (mean = 816 ± 24 mm) while upstream sites ranged from 428 mm to 1091 mm (mean = 852 ± 24 mm). Due to small sample sizes, PSD values were only calculated for Bighead Carp at the Des Moines River confluence site and at Cliffland. Bighead Carp size structure was larger at the Cliffland and smaller at Keokuk (Appendix B).

Bighead Carp mean relative weight varied among months but exhibited similar patterns of high relative weight among sites (Appendix C). Mean Bighead Carp relative weight across all sites and dates was 94 (± 1 SE). Relative weight of Bighead Carp was similar at Keosauqua (mean = 98 ± 7 SE),

Eddyville (mean = 96 ± 8 SE), Keokuk (mean = 93 ± 2 SE), and Cliffland (mean = 95 ± 2 SE). Relative weight of Bighead Carp also varied among months, as Wr generally peaked at all sites during late spring and decreased in subsequent months until it peaked again in the fall across all sites (Appendix C).

Few Silver Carp were captured in trammel nets during this study. Six trammel net sets (out of 95 total sets; 6.3%) accounted for 257 of 431 (60%) Silver Carp captured with this gear (mean CPUE in these six sets = 42.5 fish/net ± 6.3 SE). Catch rates in the remaining net sets were extremely low (mean = 24

2.0 fish/net ± 0.5 SE). Because few Silver Carp were captured with trammel nets and most sets did not capture Silver Carp (65.3% of total sets), further analyses using data collected from this gear were not conducted.

In all, 2,476 Silver Carp were captured using daytime electroshocking in the Des Moines River from April to October 2014 (1,014 Carp) and 2015 (1,462 Carp). Mean electrofishing CPUE of Silver

Carp varied between years (P < 0.001), sites (P < 0.001), months (P = 0.01), and their interactions (P <

0.001). Silver Carp catch rates were higher in 2015 (CPUE: 18.6 ± 2.8 SE) compared to 2014 (CPUE:

12.7 ± 3.0 SE). During both years, the highest CPUE consistently occurred at Keokuk and Cliffland while lower CPUEs generally occurred at Eddyville and Keosauqua (Figure 2). Monthly mean electroshocking CPUE was significantly different among monthly pairwise comparisons intra-annually, ranging from 0 to 434.0 fish per hr during 2014 and from 0 to 230.6 fish per hr during 2015 (Figure 2).

During 2014, Silver Carp CPUE at Cliffland and Keokuk increased from April to June, decreased during

June and August, and increased throughout September and October (Figure 2). Silver Carp CPUE at

Eddyville was highest during September as no individuals were captured from April through August.

Conversely, CPUE at Keosauqua increased from May to June and were lower the remainder of the year.

During 2015, Silver Carp CPUE at Cliffland and Keokuk peaked during April and decreased throughout the year until a slight increase in CPUE during September. In 2015, CPUE at Eddyville peaked during

June and was sustained from June through September until a sharp decline during October. Finally,

Silver Carp CPUE at Keosauqua increased from April to July and declined markedly after thereafter.

Silver Carp CPUE was positively related to mean daily discharge (r = 0.07 - 0.75 for all sites;

Figure 3). Silver Carp CPUE was positively related to mean daily discharge at both Eddyville (r = 0.60,

P = 0.004) and Cliffland (r = 0.75, P = 0.01) while it was not significantly related to CPUE at Keosauqua

(r = 0.07, P = 0.23) or Keokuk (r = 0.14, P = 0.26). Additionally, Pearson’s correlation coefficients were lowest at the farthest downstream site (Keokuk) and highest for the farthest upstream site (Eddyville). In contrast, neither water temperature nor conductivity were related to CPUE across all sites (P > 0.10 for all correlations; Figure 3). 25

Silver Carp size structure was generally larger at downstream sites compared to upstream sites.

Silver Carp ranged 491 to 917 mm (mean = 671 mm) and 1.3 to 9.9 kg (mean = 3.2 kg) at Keokuk, 535 to

885 mm (mean = 664 mm) and 1.3 to 7.1 kg (mean = 3.1 kg) at Keosauqua, 450 to 887 mm (mean = 626 mm) and 1.0 to 8.2 kg (mean = 2.4 kg) at Cliffland, and 551 to 826 mm (mean = 641 mm) and 1.5 to 6.7 kg (mean = 2.6 kg) at Eddyville. Preferred size Silver Carp composed 91% of total catches followed by memorable and quality sizes. Size structure was similar among months at all sites with the exception of

Cliffland where a greater proportion of quality length Silver Carp were collected from August through

October compared to samples collected from April through July (Figure 4).

Silver Carp relative weight varied spatially and temporally throughout the Des Moines River.

Mean Silver Carp relative weight was 91 (± 0.001 SE) and was similar among length groups (F2, 2315 =

0.41, P = 0.67). However, there was significant between-year variation (F1, 2315 = 181.61, P = <0.0001), as Silver Carp captured during 2014 had higher relative weight (mean = 95 ± 0.004 SE) compared to fish captured from 2015 (mean = 91 ± 0.003 SE). Silver Carp relative weight also varied among sites (F3, 2315

= 93.028, P <0.0001) and decreased from downstream to upstream sites (higher at Keokuk [mean = 97 ±

0.5 SE] and Keosauqua [mean = 93 ± 0.9 SE] compared to Cliffland [mean = 87 ± 0.4 SE] and Eddyville

[mean = 91 ± 0.6 SE]). Silver Carp relative weight also varied among months (F1, 2315 = 428.9, P <

0.0001) and the interaction between site and month (F1, 2315 = 7.81, P < 0.0001), generally peaking during late spring and decreasing in subsequent months (Figure 5). Silver Carp relative weight at Eddyville was higher during the spring and significantly decreased throughout the year. However, Silver Carp relative weight collected during 2015 peaked during April as Silver Carp were not captured during May. At

Cliffland, Silver Carp relative weight peaked during late spring and early summer and decreased during the fall. Additionally, mean relative weight of Silver Carp increased after May until peaking during July

2014 (Figure 5). Despite only capturing >5 fish during four months, relative weight of Silver Carp captured at Keosauqua peaked during May and decreased throughout the summer. Finally, mean relative weight of Silver Carp captured at Keokuk exhibited a bimodal peak, as peaks were present during April and August 2014 (Figure 5). 26

Discussion

My results demonstrate the degree of seasonal variability in Silver Carp population characteristics within a major Mississippi River tributary where Silver Carp have persisted since the 1990s (NAS 2016).

Seasonal trends in Silver Carp catch rates and relative weight supported my hypotheses that catch rates would be highest during the spring and fall months and relative weight would be highest during the spring, both in response to spring spawning activity as well as fall movement patterns (Coulter et al.

2016). In contrast, size structure was similar throughout the year at three of four sites, suggesting a lack variation in Silver Carp size structure intra-annually. Similar seasonal variations of fish sampling dynamics have been described for a suite of freshwater species, with an emphasis on native species and sportfishes (e.g., Pope and Willis 1996; Miller and Scarnecchia 2008; Bacula et al. 2011; Bowlby and

Hoyle 2011; Muhlfeld et al. 2012; Gardner et al. 2013; Herbst et al. 2015). As temporal sampling variation can hinder accurate assessments of population structure, information provided herein can aid fisheries biologists seeking to monitor and manage Silver Carp populations effectively.

Across both years, Silver Carp catch rates varied intra-annually at three (Eddyville, Cliffland, and

Keokuk) out of the four sites sampled in the Des Moines River, where spring and fall catch rates were generally highest. Increases in catch rates during spring may be attributed to upstream spawning migrations of Silver Carp. In major Mississippi River tributaries, Silver Carp movements increase during the spring with increases in temperature and flow (Degrandchamp et al. 2008; Coulter et al. 2016). Upon making upstream spring migrations, Silver Carp appear to congregate near dams (Calkins et al. 2012) that may have increased local abundances, resulting in higher catch rates at upstream sites. Such upstream spawning movements have also been documented for other migratory riverine fishes (e.g., Gulf Sturgeon

Acipenser oxyrinchus desotoi; Grammer et al. 2015) as environmental conditions can cue fish migrations to staging areas, increasing local abundances temporarily. Thus, the flux of Silver Carp during spring spawning migrations appears to result in higher catch rates relative to other sampling seasons. 27

Silver Carp catch rates were generally lowest during mid- to late-summer and increased again during the late summer and fall. Silver Carp seasonal movement patterns may explain declines in catch rates during the summer. Silver Carp movement within two other Mississippi River tributaries is low during mid- to late- summer while increases in Silver Carp movements occur during fall periods in response to changing river temperatures (DeGrandchamp et al. 2008; Coulter et al. 2016). As such, lower catch rates during periods of high water temperatures within the Des Moines River could be due to Silver

Carp occupying habitats that were not sampled. Alternatively, declines in catch rates could be attributed to a decrease in electroshocking netter efficiency. Silver Carp leap out of the water in response to physical stimuli (e.g., sound, vibration, etc.; Kolar et al. 2007). Observed throughout the study, this leaping ability tended to be highly variable seasonally, as higher water temperatures appeared to increase leaping ability during daytime boat electroshocking. Such increases in leaping ability may decrease electroshocking netting efficiency and subsequently summer catch rates. Combined, the effects of decreased site occupancy and the increase in leaping ability may have resulted in lower summer catch rates relative to both spring and fall.

Mean daily discharge was positively related to Silver Carp capture rates at the two farthest upstream sites but the strength of the relationship decreased at downstream sites. At Keosauqua, Silver

Carp catch rates were generally low and at Keokuk, catch rates were generally high across nearly all sampling occasions, regardless of discharge. The lack of a relationship at these sites could be related to the nature of the hydrograph. The Mississippi River sustains a relatively stable flow compared to tributaries that have a larger magnitude of variation between maximum and minimum flows (Bhowmik and Adams 1986). The lack of extreme variation in Mississippi River discharge may provide adequate

Asian Carp habitat consistently, decreasing the fluctuations in local population abundances and causing an insignificant relationship between discharge and capture rates. In contrast, within the Des Moines

River, upstream sites are characterized by a deeper channel and steeper banks, creating river stretches where water velocity is more variable. As Silver Carp migrate in response to dramatic increases in discharge (Zhang et al. 2000; Li et al. 2006; Wang et al. 2008), migrations from downstream to upstream 28

habitats where velocity is higher during spawning may augment local Silver Carp abundances, reflected herein. As such, mean daily discharge may be a better predictor for capture rates at upstream sites compared to downstream sites.

Silver Carp size structure was similar intra-annually except at Cliffland, where catches from April through July contained a larger proportion of memorable length fish compared to August through

October. Multiple examples of seasonal variation in size structure for a variety of freshwater species have been previously documented (e.g., Bettross and Willis 1988; Mesa et al. 1990; Lott and Willis 1991;

Mero and Willis 1992). Within the current study, lack of seasonal variation in Silver Carp size structure could be explained by two phenomena. First, only trammel nets and electroshocking were used to capture

Silver Carp. Electroshocking has been documented to capture a wide size range of Silver Carp (e.g.,

McClelland and Sass 2008; Wanner and Klumb 2009a; Sass et al. 2010; Stuck 2012) while trammel nets capture larger sizes (e.g., Wanner and Klumb 2009a). In contrast, smaller juvenile Silver Carp (< 250 mm) may be more effectively captured with other passive gears (e.g., mini-fyke nets; Wanner and Klumb

2009a). The inability of both gears used to capture smaller sizes of Silver Carp could lead to underrepresentation of smaller size class fish and may have led to the lack of temporal variation in size structure. Alternatively, temporal variation in Sauger (Sander canadensis; Mero and Willis 1992),

Smallmouth Bass (Mesa et al. 1990; Bacula et al. 2011), Largemouth Bass (Micropterus salmoides;

Carline et al. 1984; Bettross and Willis 1988), and Crappie (Pomoxis spp.; Boxrucker and Ploskey 1989) size structure has been attributed to seasonal movements of adult fish between shallow and deep water and the occupation of littoral habitats by young fish during fall. However, such studies have been conducted in lentic environments that often have greater maximum and mean depths compared to lotic environments that are often shallow and constitute a substantial amount of longitudinal and latitudinal variability in morphometric characteristics. Such variations in morphometric characteristics of lotic systems do not allow for seasonal vertical migrations of adult fish as observed in lentic systems.

Additionally, Silver Carp prefer open (Abdusamadov 1987), slack water habitat (Berg 1964; Rasmussen

2002), occupy the upper layers of the water column (Shetty et al. 1989), and rarely occupy depths over 4 29

m from April through August, regardless of abiotic conditions (DeGrandchamp et al. 2008). Combined, the lack of deep-water habitats within sites and the tendency of Silver Carp to occupy shallow habitats throughout the year could have led to the lack of temporal size structure variation within the Des Moines

River.

Peaks in Silver Carp relative weight during the spring is characteristic of spawning activity and has been documented for a variety of other fishes (Pope and Willis 1996). Relative weight of Silver Carp peaked during May in both years and decreased throughout the year that may be attributed to reproductive activity. Asian Carp spawning within the Mississippi River basin (Kolar et al. 2007; Lohmeyer and

Garvey 2009; Deters et al. 2013) and my study sites (Camacho 2016) occurs throughout May and June.

After reproduction, fish tissue energy reserves are depleted and condition tends to decline (e.g.,

Henderson et al. 1995). However, these trends may not apply to immature Silver Carp. Silver Carp <450 mm were absent in my samples and could display different trends in relative weight compared to the larger, reproductively mature fish. In eastern South Dakota rivers, Silver Carp condition (Fulton’s K) was relatively stable intra- and inter-annually (Hayer et al. 2014), indicating that reproductively immature

Silver Carp lack seasonal variability in relative weight. Similarly, mature Yellow Perch (Perca flavescens) have temporally varying condition relative to immature perch where condition is constant due to the energy allocation required for gonad production prior to the spawning season (Le Cren et al. 1951).

As such, relative weight of Silver Carp > 450 mm varies intra-annually due to seasonal reproductive habits and should be taken into consideration when implementing standardized sampling strategies.

Contrary to existing literature (e.g., Wanner and Klumb 2009), trammel nets were unsuccessful at capturing Silver Carp and had lower catches relative to electroshocking. Throughout this study, electroshocking neglected to capture Silver Carp on only 6 occasions (3.9%) compared to trammel nets where 65.3% of net sets failed to capture Silver Carp. Additionally, sampling occasions where trammel net sets had high capture rates also resulted in high electroshocking catches. As such, electroshocking outperformed trammel net sets over a wide range of Silver Carp relative abundances, indicating that trammel nets offer either superfluous information or inadequately sample Silver Carp in the Des Moines 30

River. Trammel nets were set such that backwater areas that Silver Carp tend to inhabit were blocked off and electroshocking was used to push fish into the net. Throughout this process, nets were set for less than 1 hr while electroshocking the area, potentially leading to low trammel net captures. Conversely, long-term monitoring of fish communities on the Missouri River reported lower catches (as proportion of total catch) of adult Silver Carp using boat electroshocking compared to passive gears (e.g., hoop nets, bag seine, fyke-net, etc.; Wanner and Klumb 2009). However, Silver Carp abundances are variable across sites and, in some cases, are low (NAS 2016), potentially favoring passive gears that are employed for a longer duration compared to electroshocking. Consequently, fisheries managers should choose a sampling design that provides the most representative information about the extant fish population of interest. Therefore, for established populations of Silver Carp near the Mississippi River, standardized sampling protocols that use spring or fall boat electroshocking during either May or September when water temperatures are between 16°C and 22°C appear most effective.

The information provided herein will aid fisheries managers when designing methodological approaches for Silver Carp standardized sampling. In river reaches where Silver Carp are abundant (e.g.,

Illinois River, USA; Sass et al. 2009), seasonal effects could be of critical importance when implementing management strategies. Sampling for baseline population data will be most effective if carried out at times when catch rates are highest. In river reaches where Silver Carp have yet to establish or are recent invaders (e.g., Upper Mississippi River), the choice of sampling season could determine whether Silver

Carp are detected. Early detection and standardized monitoring during time frames when detection and capture probability are highest can increase the chances of enacting effective preventative and management strategies before populations become overly abundant. Additionally, if there is threat of

Silver Carp invading a new river reach, diligent sampling during either spring or fall periods offers the highest probability of detectability, potentially accelerating Silver Carp preventative management strategies. Thus, managers must consider project goals as well as the current status of Silver Carp in surrounding waterways when designing and performing Silver Carp monitoring.

Literature Cited

Abdusamadov AS (1987) Biology of White Amur (Ctenopharyngodon idella), Silver Carp (Hypophthalmichthys molitrix), and Bighead (Aristichthys nobilis), acclimatized in the Terek Region of the Caspian Basin. Journal of Ichthyology 26:41-49 Bacula TD, Blackwell BG, Willis DW (2011) Seasonal sampling dynamics of Smallmouth Bass (Micropterus dolomieu) in northeastern South Dakota. Journal of Freshwater Ecology 26:345-356 Béguer-Pon M, Castonguay M, Benchetrit J, Hatin D, Legault M, Verreault G, Mailhot Y, Tremblay V, Dodson JJ (2015) Large-scale, seasonal habitat use and movements of yellow American Eels in the St. Lawrence River revealed by acoustic telemetry. Ecology of Freshwater Fish 24:99-111 Berg LS (1964) Freshwater fishes of the USSR and adjacent countries. Volume ΙΙ. Fourth edition. Translated from Russin. The Smithsonian Institution and The National Science Foundation, Washington, DC Bettross EA, Willis DW (1988) Seasonal patterns in sampling data for Largemouth Bass and Bluegill in a northern great plains impoundment. Prairie Naturalist 20:193-202

Bhowmik NG, Adams JR (1986) The hydrologic environment of Pool 19 of the Mississippi River. Hydrobiologia 136:21-30 Bonar SA, Hubert WA (2002) Standard sampling of inland fish: benefits, challenges, and a call for action. Fisheries 27:10-16 Bowlby JN, Hoyle JA (2011) Distribution and movement of Bay of Quinte Walleye in relation to temperature, prey availability, and Dreissenid colonization. Aquatic Ecosystem Health and Management 14:56-65 Boxrucker J, Ploskey G (1989) Gear and seasonal biases associated with sampling crappies in Oklahoma. Proceedings of the Annual Conference of the Southeastern Association of Fish and Wildlife Agencies 42:89-97 Calkins HA, Tripp SJ, Garvey JE (2012) Linking Silver Carp habitat selection to flow and phytoplankton in the Mississippi River. Biological Invasions 14:949-958 Carlander KD, Lewis WM, Ruhr CE, Cleary RE (1953) Abundance, growth, and condition of Yellow Bass, Morone Interrupta Gill, in Clear Lake, Iowa, 1941 to 1951. Transactions of the American Fisheries Society 82:91-103 Carline RF, Johnson BL, Hall TJ (1984) Estimation and interpretation of proportional stock density for fish populations in Ohio impoundments. North American Journal of Fisheries Management 4:139-154 Chang WYB (1966) Culture of freshwater fish in Chine. In E.o> Gangstad, editor. 1980. Chinese fish culture. Report 1. Technical report A-79. Aquatic plant control research program. Washington, D.C. U.S. Army Waterways Experiment Station (draft translated by T.S.Y. Koo, 1980)

Collins SF, Butler SE, Diana MJ, Wahl DH (2015) Catch rates and cost effectiveness of entrapment gears for Asian Carp: A comparison of pound nets, hoop nets, and fyke nets in backwater lakes of the Illinois River. North American Journal of Fisheries Management 35:1219-1225

Conover GR, Simmonds WM (2007) Management and control plan for Bighead, Black, Grass, and Silver Carps in the United States. Asian Carp Working Group, Aquatic Nuisance Species Task Force, Washington, D.C.

Coulter AA, Bailey EJ, Keller D, Goforth RR (2016) Invasive Silver Carp movement patterns in the predominantly free-flowing Wabash River (Indiana, USA). Biological Invasions 18:471-485

Coulter AA, Keller D, Amberg JJ, Bailey EJ, Goforth RR (2013) Phenotypic plasticity in the spawning traits of Bigheaded Carp (Hypophthalmichthys spp.) in novel ecosystems. Freshwater Biology 58:1029-1037

Cowley DE, Wissmar RC, Sallenave R (2007) Fish assemblages and seasonal movements of fish in irrigation canals and river reaches of the middle Rio Grande, New Mexico (USA). Ecology of Freshwater Fish 16:548-558

DeGrandchamp KL, Garvey JE, Csoboth LA (2007) Linking adult reproduction and larval density of invasive Carp in a large river. Transactions of the American Fisheries Society 136:1327-1334 DeGrandchamp KL, Garvey JE, Colombo RE (2008) Movement and habitat selection by invasive Asian Carps in a large river. Transactions of the American Fisheries Society 137:45-56 Deters JE, Chapman DC, McElroy B (2013) Location and timing of Asian Carp spawning in the lower Missouri River. Environmental Biology of Fishes 96:617-629 Gabelhouse DW, et al (1992) Fish sampling and data analysis techniques used by conservation agencies in the U.S. and Canada. Fisheries Techniques Standardization Committee, Fisheries Management Section, American Fisheries Society, Bethesda, MD. Gardner CJ, Deeming DC, Eady PE (2013) Seasonal movements with shifts in lateral and longitudinal habitat use by Common Bream, Abramis brama, in a heavily modified lowland river. Fisheries Management and Ecology 20:315-325. Gardner W, Mulvey EP, Shaw EC (1995) Regression analysis of counts and rates: Poisson, overdispersed Poisson, and negative binomial models. Psychological Bulletin 118:392-404 Garvey JE, DeGrandchamp KL, Williamson CJ (2006) Life history attributes of Asian Carps in the upper Mississippi River system. Reports. Paper 3. http://opensiuc.lib.siu.edu/fiaq_reports/3 Grammer PO, Mickle PF, Peterson MS, Havrylkoff JM, Slack WT, Leaf RT (2015) Activity patterns of Gulf Sturgeon (Acipenser oxyrinchus desotoi) in the staging area of the Pascagoula River during fall outmigration. Ecology of Freshwater Fish 24:553-561 Hayer CA, Graeb BD, Bertrand KN (2014a) Adult, juvenile and young-of-year Bighead, Hypophthalmichthys nobilis (Richardson, 1845) and Silver Carp, H. molitrix (Valenciennes, 1844) range expansion on the northwestern front of the invasion in North America. BioInvasional Records 3:283-289 Hayer CA, Breeggemann JJ, Klumb RA, Graeb BD, Bertrand KN (2014b) Population characteristics of Bighead and Silver Carp on the northwestern front of their North American invasion. Aquatic Invasions 9:289-303 Henderson BA, Wong JL, Nepszy SJ (2005) Reproduction of Walleye in Lake Erie: allocation of energy. Canadian Journal of Fisheries and Aquatic Sciences 53:127-133 33

Herbst SJ, Stevens BS, Hayes DB, Hanchin PA (2015) Estimating Walleye (Sander vitreus) movement and fishing mortality using state-space models: implications for management of spatially structure populations. Canadian Journal of Fisheries and Aquatic Sciences 73:330-348 Irons KS, Sass GG, McClelland MA, Stafford JD (2007) Reduced condition factor of two native fish species coincident with invasion of nonnative Asian Carps in the Illinois River, U.S.A. Is this evidence for competition and reduced fitness? Journal of Fish Biology 71:258-273 Jones MJ, Stuart IG (2009) Lateral movement of Common Carp (Cyprinus carpio L.) in a large lowland river and floodplain. Ecology of Freshwater Fish 18:72-82 Kaul M, Rishi KK (1993) Exotic Chinese Carps. Punjab Fisheries Bulletin 27:53-56

Koel TM, Irons KS, Ratcliff E (2000) Asian Carp invasion of the Upper Mississippi River System. Upper Midwest Environmental Sciences Center, Project Status Report Kolar CS, Lodge DM (2002) Ecological predictions and risk assessment for alien species. Science 298:1233-1236 Krykhtin ML, Gorbach EI (1981) Reproductive ecology of the Grass Carp, Ctenopharyngodon idella, and the Silver Carp, Hypophthalmichthys molitrix, in the Amur Basin. Journal of Ichthyology 21:109- 123 Lamer JT, Dolan CR, Petersen JL, Chick JH, Epifanio JM (2010) Introgressive hybridization between Bighead Carp and Silver Carp in the Mississippi and Illinois rivers. North American Journal of Fisheries Management 30:1452-1461 Le Cren ED (1951) The length-weight relationship and seasonal cycle in gonad weight and condition in the Perch (Perca fluviatilis). Journal of Animal Ecology 20:201-219 Li C, Peng J, Liao W (2006) Study on the eco-hydrological factors and flow regime requirements on spawning of four major Chinese Carps in the middle reaches of the Yangtze River. Journal of China Institute of Water Resources and Hydropower Research 14:170-176 Lohmeyer AM, Garvey JE (2009) Placing the North American invasion of Asian Carp in a spatially explicit context. Biological Invasions 11:905-916 Lott FE, Willis DW (1991) Gill net mesh size efficiency for Yellow Perch. Prairie Naturalist 23: 139-144

Lott JP (2000) Smallmouth Bass movement, habitat use and electrofishing susceptibility in lower lake Oahe, South Dakota. Pierre: South Dakota Game, Fish and Parks, Wildlife Division. Annual Report 00-15 McClelland MA, Sass GG (2008) The long-term Illinois River fish population monitoring program. Illinois Natural History Survey, Technical Report Mckibbin WL (2002) Structure and dynamics of Largemouth Bass populations in eastern South Dakota glacial lakes and large impoundments. [Master’s thesis]. [Brookings]: South Dakota State University Mero SW, Willis DW (1992) Seasonal variation in sampling data for Walleye and Sauger collected with gill nets from Lake Sakakawea, North Dakota. Prairie Naturalist 24:231-240

Mesa MG, Duke SD, Ward DL (1990) Spatial and temporal variation in proportional stock density and relative weight of Smallmouth Bass in a reservoir. Journal of Freshwater Ecology 5:323-339

Miller SE, Scarnecchia DL (2008) Adult Paddlefish migrations in relation to spring river conditions of the Yellowstone and Missouri rivers, Montana and North Dakota, USA. Journal of Applied Ichthyology 24: 221-228 Mooney HA, Hobbs RJ (2000) Invasive species in a changing world: Washington D.C., Island Press 457 Muhlfeld CC, Giersch JJ, Marotz B (2012) Seasonal movements of non-native Lake Trout in a connected lake and river system. Fisheries Management and Ecology 19:224-232 NAS (2016) Hypophthalmichthys molitrix (Silver Carp). Nonindigenous Aquatic Species. http://nas.er.usgs.gov/queries/SpeciesAnimatedMap.aspx?speciesID=549 Neal JW, Prchalová M (2012) Spatiotemporal distributions of Threadfin Shad in tropical reservoirs. North American Journal of Fisheries Management 32:929-940 Papoulias DM, Chapman D, Tillitt DE (2006) Reproductive condition and occurrence of intersex in Bighead and Silver carp in the Missouri River. Hydrobiologia 571:355-360 Phelps QE, Willis DW (2013) Development of an Asian Carp size structure index and application through demonstration. North American Journal of Fisheries Management 33:338-343 Pope KL, Willis DW (1996) Seasonal influences on freshwater fisheries sampling data. Reviews in Fisheries Science 4:57-73 Pope KL, Kruse CG (2007) Condition. En: Guy, C.S. and M.L. Brown, ed. Analysis and Interpretation of Freshwater Fisheries Data. American Fisheries Society Publication Rasmussen JL (2002) The Cal-Sag and Chicago Sanitary and Ship Canal: a perspective on the spread and control of selected aquatic nuisance fish species. U.S. Fish and Wildlife Service, Region 3 White Paper, Fisheries Resource Office, Rock Island, Illinois. 26pp Ruetz III CR, Uzarski DG, Krueger DM, Rutherford ES (2006) Sampling a littoral fish assemblage: comparison of small-mesh fyke netting and boat electrofishing. North American Journal of Fisheries Management 27:825-831 Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O'Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Annual Review of Ecology and Systematics 32:305-332 Sampson SJ, Chick JH, Pegg MA (2009) Diet overlap among two Asian Carp and three native fishes in backwater lakes on the Illinois and Mississippi rivers. Biological Invasions 11:483-496 Sass GG, Cook TR, Irons KS, McClelland MA, Michaels NN, O’Hara TM, Stroud MR (2010) A mark- recapture population estimate for invasive Silver Carp (Hypophthalmichthys molitrix) in the La Grange Reach, Illinois River. Biological Invasions 12:433-436 Schrank SJ, Braaten PJ, Guy CS (2001) Spatiotemporal variation in density of larval Bighead Carp in the lower Missouri River. Transactions of the American Fisheries Society 130:809-814 Schrank SJ, Guy CS (2002) Age, growth, and gonadal characteristics of adult Bighead Carp, Hypophthalmichthys nobilis, in the lower Missouri River. Environmental Biology of Fishes 64:443-450 Seibert JR, Phelps QE, Yallaly KL, Tripp S, Solomon L, Stefanavage T, Herzog DP, Taylor M (2015) Use of exploitation simulation models for Silver Carp (Hypophthalmichthys molitrix) populations in several Midwestern U.S. rivers. Management of Biological Invasions 6: 295-302 35

Shetty HPC, Nandeesha MC, Jhingran AG (1989) Impact of exotic aquatic species in Indian waters. Pages 45-55 in De Silva, editor. Exotic aquatic organisms in Asian. Proceedings of the workshop on introduction of exotic organisms in Asian. Asian Fisheries Society Special Publication 3 Sterner V, Bowman R (2006) Fish community monitoring of off-channel habitat at the Tieville-Decatur Bend, Louisville Bend, Tyson Bend and California Bend. Missouri River Fish and Wildlife Mitigation Project, Progress Report 2006. Prepared for the U.S. Army Corps of Engineers. Iowa Department of Natural Resources, Onawa, Iowa Stuck JG, Porreca AP, Wahl DH, Colombo RE (2015) Contrasting population demographics of Invasive Silver Carp between an impounded and free-flowing river. North American Journal of Fisheries Management 35:114-122 Tripp S, Garvey JE (2011) Fish passage in the upper Mississippi River system. Fisheries and Illinois Aquaculture Center Department of Zoology Southern Illinois University, Annual report Tripp SE, Brooks R, Herzog D, Garvey J (2013) Patterns of fish passage in the upper Mississippi River. River Research and Applications 30:1056-1064 Verigin BV, Makeyeva AP, Zaki Mokhamed MI (1978) Natural spawning of the Silver Carp (Hypophthalmichthys nobilis), the Bighead Carp (Aristichthys nobilis), and the Grass Carp (Ctenopharyngodon idella) in the Syr-Dar’ya River. Journal of Ichthyology 18:143-146

Wanner GA, Klumb RA (2009a) Asian Carp in the Missouri River: Analysis from multiple Missouri River habitat and fisheries programs. National Invasive Species Council materials. Paper 10 National Invasive Species Council materials. Paper 10 Wanner GA, Klumb RA (2009b) Length-weight relationships for three Asian Carp species in the Missouri River. Journal of Freshwater Ecology 24:489-495 Williamson CJ, Garvey JE (2005) Growth, fecundity, and diets of newly established Silver Carp in the middle Mississippi River. Transactions of the American Fisheries Society 134:1423-1430 Yi B, Yu Z, Liang Z, Sujuan S, Xu Y, Chen J, He M, Liu Y, Hu Y, Deng Z, Huang S, Sun J, Liu R, Xiang Y (1988) The distribution, natural conditions, and breeding production of the spawning ground on main stream of Yangtze River. In: Yi B, Yu Z, Liang Z (eds) Gezhouba water control project and four famous fishes in the Yangtze River. Hubrei Science and Technology Press, Wuhan:1-46

Zhang G, Chang J, Shu G (2000) Application of factor-criteria system reconstruction analysis in the reproduction research on Grass Carp, Black Carp, Silver Carp, and Bighead in the Yangtze River. International Journal of General Systems 29:419-428

Zimmer M, Schreer JF, Power M (2010) Seasonal movement patterns of Credit River Brown Trout (Salmo trutta). Ecology of Freshwater Fish 19:290-299

Tables and Figures

Figure 1. Locations of the four Des Moines River, USA sampling sites used to assess Silver Carp seasonal sampling variation. 37

Figure 2. Silver Carp electroshocking catch-per-unit-effort (CPUE; fish per hour; mean ± SE) from April through October at Eddyville, Cliffland, Keosauqua, and Keokuk during 2014 (black circle) and 2015 white circle). Points with similar letters represent CPUEs that are not significantly different (ɑ = 0.05) for both 2014 (letters a through e) and 2015 (letters w through z).

Figure 3. Pearson correlations of mean daily discharge (m3/s), water temperature (°C), and conductivity

(μS/cm) with Silver Carp monthly log catch-per-unit-effort (CPUE; fish per hour) captured from

Eddyville, Cliffland, Keosauqua, and Keokuk during 2014-2015. 39

Figure 4. Silver Carp proportional size distribution (stock 250 – 449.9 mm; quality 450 – 559.9 mm; preferred 560 – 739.9 mm; memorable 740 – 929.9 mm; trophy ≥ 930 mm; Phelps and Willis 2013) by month for fish collected at Eddyville, Cliffland, Keosauqua, and Keokuk during 2014-2015. Bars with similar letters represent proportional size distributions that are not significantly different (ɑ = 0.05). 40

Figure 5. Silver Carp relative weight (Wr; mean ± 1 SE) by sampling month at Eddyville, Cliffland,

Keosauqua, and Keokuk during 2014 (black circles) and 2015 (white circles). Points with similar letters represent Wr values that are not significantly different (ɑ = 0.05) for 2014 (letters a through e) and 2015

(letters w through z). Mean Wr was only calculated when >5 Silver Carp were captured.

CHAPTER 3. FACTORS REGULATING YEAR-CLASS STRENGTH OF SILVER CARP

THROUGHOUT NORTH AMERICA

Abstract

Recruitment of many fish populations is inherently highly variable inter-annually and synchronous fluctuations among years can occur at broad geographic scales. Fish dispersal and climatic variation (Moran effect) are two key factors thought to synchronous recruitment. Herein, I investigated the role of climatic factors in inducing synchronous recruitment of Silver Carp Hypophthalmichthys molitrix across the Missouri, Des Moines, Mississippi, Wabash, and Illinois rivers. Relative year-class strength of nine populations was indexed using year-class residuals, correlated among sites to evaluate synchrony, and related to local- and regional-scale climatic conditions. Silver Carp recruitment was asynchronous (mean ρ = -0.08 ± 0.13 SE) across the Mississippi River watershed. Populations <300 river km apart were synchronized but populations further apart or in relation to linear distance were asynchronous, suggesting dispersal may be occurring at local scales but local environmental conditions are more important determinants of recruitment at larger scales. Generally, Silver Carp recruitment was negatively related to variability in river discharge (6 of 9 populations) and positively related to cumulative river discharge (7 of 9 populations) during the reproductive period, indicating that extended periods of elevated river discharge are important local environmental factors regulating recruitment. Regionally,

Silver Carp recruitment was not related to the North Atlantic Oscillation Index, El Niño Southern

Oscillation Index, or Palmer Hydrological Drought Index, indicating that local-environmental factors have more influence on Silver Carp year-class strength than broad climatic conditions. My results suggest that Silver Carp populations across the Mississippi River watershed asynchronously recruit as a result of localized river hydrology, adding to our understanding of recruitment dynamics of a highly invasive species throughout North America.

Introduction

Spatio-temporal patterns of population fluctuations and the processes regulating them have long been a major focus of aquatic population ecology. Fish recruitment into the adult population can be highly variable inter-annually due to the sensitivity of early life-stages to fluctuations in environmental conditions (Hjort 1926). Drivers of recruitment variation are often numerous and vary across systems, combining the cumulative interactions between abiotic and biotic factors such as temperature (e.g.,

Henderson and Corps 1997), river discharge (Zorn and Nuhfer 2007), prey availability (e.g., Adams et al.

1982; Dettmers et al. 2003), and reservoir retention (e.g., Maceina 1997). As such, examining mechanistic processes regulating recruitment among fish populations can provide valuable insight into factors responsible for population fluctuations.

Despite the high degree of variability in recruitment within and among fish populations, the occurrence of synchronously fluctuating populations is now considered a common ecological phenomenon (Ranta et al. 1998) often driven by inter-annual variation in regional climatic conditions

(Henderson and Corps 1997; Phelps et al. 2008; Dembkowski et al. 2016; Honsey et al. 2016) and dispersal (Lande et al. 1999; Kendall et al. 2000). The effect of stochastic climatic perturbations on the synchronization of recruitment (i.e., Moran effect; Moran 1953) has been largely studied in spatially distinct populations, such as Cisco Coregonus artedi (Myers et al. 2015), Yellow Perch Perca flavescens

(Dembkowski et al. 2016; Honsey et al. 2016), and Common Carp Cyprinus carpio (Phelps et al. 2008), across broad geographic ranges. Alternatively, the synchronization of fish recruitment can be locally restricted and augmented through dispersal (e.g., Haydon and Steen 1997), especially with either highly migratory species or interconnected populations (Goldwyn and Hastings 2011). Hence, determining the degree and relative influence of regional climatic patterns or dispersal on recruitment synchrony over broad geographic areas can add valuable insights into the nature of fish population fluctuations.

The spatial extent of synchronous fluctuations in fish recruitment has been evaluated among both marine and freshwater environments and generally indicates that synchrony decreases with increasing 43

distance between populations (Myers et al. 1997; Koenig 1999; Tedesco et al. 2004; Honsey et al. 2016).

Within marine environments, most fishes display patterns of synchronous recruitment at distances nearing

500 km (Myers et al. 1997; Pyper et al. 2001) whereas synchrony within freshwater species is generally

50 km or less (Myers et al. 1997). However, more recent examples suggest that synchronous recruitment of some lentic freshwater fishes can exceed 50 km (Phelps et al. 2008; Dembkowski et al. 2016; Honsey et al. 2016). For instance, Yellow Perch populations synchronously recruit at scales greater than 150 km within the Lacustrine Great Lakes (Honsey et al. 2016) and Prairie Pothole Region (Dembkowski et al.

2016). Similarly, Common Carp populations in the Prairie Pothole Region exhibited synchronous recruitment across a 175 km2 area (Phelps et al. 2008). Although the extent that freshwater fish species synchronously recruit is highly variable, the spatial extent of synchrony is reduced compared to marine systems, potentially attributable to the strong influence of local biotic factors on early life stages (Myers et al. 1997) or lack of dispersal potential (e.g., Dembkowski et al. 2016).

Synchronous recruitment of freshwater fishes appears to be influenced by regional stochastic climatic events (e.g., Phelps et al. 2008; Bunnell et al. 2016; Honsey et al. 2016). Among lentic systems, similarities in hydrological variables (Dembkowski et al. 2016), water temperature (Bunnell et al. 2010;

Honsey et al. 2016), wind patterns, or a combination of these variables (Phelps et al. 2008; Bunnell et al.

2016) have been suggested to synchronize recruitment. Within lotic systems, synchronous recruitment is largely dependent upon hydrological variables, including discharge during fry emergence (Cattanéo et al.

2003) and the variability in annual discharge (Tedesco et al. 2004), in addition to large scale variation in water temperature (Grenouillet et al. 2001). However, regional synchrony in lotic systems has generally only been evaluated at small spatial scales (<200 km, Zorn and Nuhfer 2007; but see Cattanéo et al.

2003). Thus, the extent to which abiotic factors or dispersal influence the synchronization of fish populations in larger, interconnected systems at broader spatial scales remains largely unknown.

The Mississippi River is the largest drainage system in North America and has long been used as a means of transportation, maintained by the construction of levees, locks and dams, and weirs, altering 44

the natural flow regime. As a result, fish access to important floodplain habitat is limited, oftentimes unpredictable, and highly dependent upon river levels, driven by precipitation patterns and dam operations throughout the basin. Fishes that use floodplain habitats for reproduction are dependent upon large-scale flood events to allow access to such habitats, promoting year-class success (Junk et al. 1989;

Janáč et al. 2010; Miyazono et al. 2010). Consequently, large-scale recruitment synchrony among different fish populations within the Mississippi River basin may be occurring during high discharge events that reconnect the Mississippi River and its associated tributaries to floodplain habitat.

In addition to habitat modifications, aquatic communities inhabiting the Mississippi River basin have been significantly altered due to a multitude of biological invasions (NAS 2016). Such invasions are increasing in frequency at an alarming rate (e.g., Ruiz et al. 1999), where the recent invasion of Silver

Carp Hypophthalmichthys molitrix has elicited substantial concern among ecologists and recreational user groups alike. Since their introduction into a Mississippi River tributary in the mid-1970s (Freeze and

Henderson 1982), Silver Carp have quickly established and become ubiquitous across much of the

Mississippi River watershed. Silver Carp life history attributes (e.g., rapid growth, early maturation, high fecundity, broad diets; Schrank and Guy 2002; Williamson and Garvey 2005; Garvey et al. 2006;

Papoulias et al. 2006) and ability to tolerate a wide range of environmental factors (e.g., temperature, turbidity, water quality; see Kolar et al. 2007) have aided in their successful establishment and subsequent expansion into much of the Mississippi River watershed. In addition, these characteristics allow Silver

Carp to attain high densities and negatively alter environments through cascading trophic effects in novel systems (e.g., Irons et al. 2007). Yet, limited knowledge exists detailing large-scale recruitment patterns and associated abiotic environmental factors influencing Silver Carp year-class success.

Silver Carp are a highly mobile species (DeGrandchamp et al. 2008; Coulter et al. 2016) and processes such as source-sink dynamics are thought to regulate populations (Hayer et al. 2014). Thus, fish dispersal from downstream to upstream habitats has the ability to synchronize recruitment. In contrast, large-scale spatial synchrony resulting from similarities in broad scale environmental conditions 45

has recently received substantial attention but has yet to be evaluated for Silver Carp. Across native and invasive ranges, Silver Carp typically spawn in rapidly flowing river segments (thalweg habitats; 0.6-2.3 m/s) in conjunction with temperatures ranging from 18-30°C (Chang 1966; Verigin et al. 1978; Kaul and

Rishi 1993; Camacho 2016). In addition, sudden increases in river discharge serve as a cue for Silver

Carp spawning (Krykhtin and Gorbach 1981; Yi et al. 1988; Zhang et al. 2000; Garvey et al. 2006; Li et al. 2006; DeGrandchamp et al. 2007; Wang et al. 2008; Deters et al. 2013) and recruitment may be low when these hydrological conditions are not met (Lohmeyer and Garvey 2009). Thus, spatial and temporal variation in conditions necessary for successful spawning may synchronize Silver Carp recruitment throughout the Mississippi River basin.

Investigating the role of environmental perturbations in synchronizing population fluctuations can aid in the understanding of recruitment of Silver Carp populations. Therefore, the objectives of my study were to (1) determine if recruitment among Silver Carp populations in the Missouri, Des Moines,

Mississippi (middle and lower river reaches), Illinois, and Wabash rivers is synchronized, (2) estimate the extent of spatial scale for recruitment synchrony, if found, and (3) examine the role of abiotic factors

(both local and regional) in regulating Silver Carp recruitment. I hypothesized that fluctuations in Silver

Carp recruitment would be synchronized among adjacent populations due to similarities in river discharge

(e.g., high water periods) and temperature patterns (e.g., warmer spring/summer conditions) while regional-climatic patterns that lead to warmer and wetter summers would improve Silver Carp year-class strength. Ultimately, this study will further our understanding of local and regional mechanistic processes influencing Silver Carp year-class success.

Materials and Methods

Study Area

With origins at Lake Itasca in northern Minnesota, the Mississippi River is the largest river in the

United States, flowing 3,732 km south to the Gulf of Mexico and creating borders for 10 states. In total, 46

the Mississippi River drains nearly 41% of the contiguous United States covering approximately 3.2 million km2 with a mean annual discharge of 18,400 m3/s. Throughout the watershed, the river encompasses a variety of anthropocentric alterations and has a myriad of tributaries that intersect varying landscapes. Several major watersheds, including the Missouri, Des Moines, Illinois, and Wabash rivers, collectively make up the Mississippi River basin. The Missouri River flows from western Montana for

3,767 km to its confluence at St. Louis, Missouri, draining a total area of roughly 1.3 million km2. Since the 1900s, the Missouri River has undergone modifications such as channelization, dam construction, and bank stabilization, altering the natural flow regime. The Des Moines River has its origin in Lake Shetek,

Minnesota and flows 845 km to the confluence of the Mississippi River at Keokuk, Iowa. In total, the

Des Moines River drains an area of 40,940 km2 with a mean daily discharge of 232 m3/sec (USGS 2013).

Along the Des Moines River, Red Rock dam was completed in 1969 and Saylorville dam was completed in 1977 for flood control purposes and operate in unison to prevent flood related damages in Des Moines,

Ottumwa and Keosauqua, Iowa and Quincy, Illinois. The Illinois River basin originates in southern

Wisconsin and western Indiana at the convergence of the Kankakee and Des Plaines rivers, flowing a total distance of 439 km and draining an area of 72,701 km2. Similar to the Missouri and Des Moines rivers, dams and river channelization projects have been completed along the Illinois River, creating an unnaturally pooled and regulated hydrograph upstream and a seemingly more natural hydrograph in farthest downstream portions where floodplain habitats disperses flood waters. Finally, the Wabash River originates in western Ohio and flows 810 km southwest to where it forms the Indiana-Illinois border prior to draining into the Ohio River near Mt. Vernon, Indiana, draining nearly 103,600 km2 with a mean daily discharge of 1,000 m3/sec. Differing from many major Mississippi River tributaries, the Wabash River contains nearly 661 river km of free-flowing river downstream from its’ single mainstem dam near

Huntington, Indiana. In all, the selected study systems are widespread across the Mississippi River watershed, encompassing a large diversity of local environmental influences which could influence and regulate Silver Carp year-class success. 47

Field Sampling

Silver Carp were captured from June through September 2015 at nine locations from four major

Mississippi River tributaries (Des Moines, Illinois, Missouri, and Wabash rivers) as well as the lower and middle Mississippi River (Table 1; Figure 1). At each site, approximately 100 Silver Carp were captured using daytime boat electroshocking (DC; 4-13 amps, 100-500 V, 60 pulses per second with two netters) focused on side channel, channel border, and backwater habitats (e.g., McClelland and Sass 2008;

Wanner and Klumb 2009; Sass et al. 2010; Stuck et al. 2015). Silver Carp were measured (total length; 1 mm) and lapilli otoliths were removed and processed for age analysis. A 1-mm thick cross section at the nucleus was cut at the anterior portion of the otolith perpendicular to the blade using a Buehler Isomet low-speed saw. Wetted 2,000-grit sandpaper was used to polish each side of the cross section. The section was then placed in immersion oil to improve clarity and annuli viewed under a dissecting microscope with transmitted light (Seibert and Phelps 2013). Lapillus otoliths were independently aged by two experienced readers with no knowledge of fish length, estimated age of the other otolith, or source river. If the readers disagreed, then a common age was decided in unison.

Environmental Data

To assess the relationship between climatic variables and Silver Carp recruitment patterns, water temperature and river discharge were obtained from United States Geological Survey (USGS; https://www.usgs.gov/) and National Oceanic and Atmospheric Administration (NOAA; https://www.ncdc.noaa.gov/) gaging stations within the Mississippi, Des Moines, Wabash, Ohio, Illinois, and Missouri river basins from 2002 to 2010. Cumulative seasonal river discharge (m3/s; May and June

[Silver Carp reproductive season (DISR)] and July through October [non-reproductive season (DISNR)]) as well as the cumulative coefficient of variation of the mean daily discharge (COVR) for the reproductive season was calculated. Discharge variables were selected on the basis that Silver Carp often spawn in response to acute increases in river flow (Verigin et al. 1978; Lohmeyer and Garvey 2009) at temperatures above 17°C (distinguishing the beginning of the reproductive season; Chang 1966; Verigin 48

et al. 1978; Kaul and Rishi 1993; Camacho 2016). Although Silver Carp are generally believed to spawn during a rising limb of discharge (Abdusamadov 1987; Kocovsky et al. 2012), Silver Carp in the Upper

Mississippi River have also been documented to reproduce on the declining limb of discharge (Camacho

2016). Thus, I included both magnitude and variability of river discharge in the model.

In addition to river discharge, regional summaries of cumulative air degree days over 17°C

(ADD), winter severity (WS), and summer severity (SS) metrics were calculated using data derived from

NOAA monitoring stations. Air temperatures are highly correlated with water temperatures across systems (Chezik et al. 2014a; Chezik et al. 2014b) and were used as a surrogate for river thermal environments. ADD was calculated as the cumulative air degree days above 17°C each year and was chosen to indicate larval fish growth potential during the first growing season. WS was calculated as cumulative air degree days below 0°C after the first growing season (Phelps et al. 2008) and was chosen to evaluate the importance of overwinter survival of young-of-the-year (YOY) Carp. Silver Carp preferred temperatures extends upwards to 26.9°C (Kolar et al. 2007) and air temperatures in the Midwest typically exceed this threshold for extended period of time. Additionally, as YOY Silver Carp seek shallow, backwater, nursery habitats during the summer months post-hatch (Kolar et al. 2007), severe increases in air temperatures as indicated by SS can cause such habitats to exceed the upper temperature threshold for YOY Carp, potentially causing high mortality rates of cohorts. Hence, summer severity was calculated as the cumulative air degree days over 27°C.

Three indices of climatic conditions were evaluated to assess relationships between broad-scale climatic variables and Silver Carp recruitment patterns across the Mississippi River watershed: North

Atlantic Oscillation (NAO) index, El Niño Southern Oscillation Index (ENSO), and the Palmer

Hydrological Drought Index (PHDI). The NAO is highly dependent upon the seasonal movements of two pressure centers over the North Atlantic as fluctuations in these features significantly alter jet stream alignments, ultimately influencing temperature regimes and precipitation distributions over a broad geographic range (Hurrell 1995). ENSO involves fluctuating ocean temperatures in the equatorial Pacific 49

where a cool phase causes less precipitation and warmer winter temperatures and warm phases are associated with more precipitation and cooler winters within the United States (Zhang et al. 1997). Last, the PHDI indicates the severity of a wet or dry period, ranging from greater than 4 (indicating extreme wetness) to less than negative 4 (indicating extreme drought; Heim 2002).

Data Analysis

Synchrony of Silver Carp recruitment throughout the Mississippi River watershed was tested for spatial autocorrelation (Koenig 1999) as well as the effects of regional, weather induced random effects

(referred to as the Moran effect; Moran 1953). Silver Carp age-frequency distributions for each river were used to evaluate past recruitment patterns and the residual method was used to quantify year-class strength or weakness using weighted catch-curve regressions (Maceina 1997). In addition, recruitment variability index (RVI; Guy and Willis 1995) was calculated to index Silver Carp recruitment variability among sites. Bivariate comparisons of Spearman’s rank correlation coefficient (ρ) between residual values were calculated to evaluate similarities in year-class strength (see Appendix D). Due to the lack of overlap in year-classes present (less than three year-classes overlap), year-class residuals from two sites

(Missouri and middle Illinois rivers) were unable to be correlated among sites and were not evaluated for synchrony among sites (correlation coefficients [ρ] vs. distance). A one-tailed, one sample t-test was conducted to test whether mean bivariate combination values among all pairs were greater than zero, which would denote synchronous population fluctuations (Honsey et al. 2016). Average ρ (± 95% confidence intervals) of residual values were regressed against both river (0-299.9, 300-599.9, 600-899.9, and >900 rkm) as well as linear (0-199.9, 200-399.9, 400-599.9, and >600 km) distance categories (Oden and Sokal 1986; Koenig and Knops 1998) to determine the spatial extent of synchrony as well as the influence of both dispersal and environmental variables on year-class strength. Length of the distance category was chosen in order to retain reasonable sample sizes of comparable magnitude within each length bin. If confidence intervals overlap zero in a given distance category, synchrony does not occur at 50

that spatial scale. In addition, I estimated the spatial scale of synchrony using the e-folding scale calculated as

푑 − ρ(푑) = ρ0푒 푣

where ρ0 is the correlation between two datasets at zero separation, d is the great-circle distance between two sites, and v is the e-folding scale (Myers et al. 1997).

Next, the effects of local, weather induced random effects on dynamic rates (the Moran effect) among Silver Carp populations were evaluated. A generalized linear mixed effects model using all possible model combinations (n=64) was used to explore the relationships between year-class strength

(residuals) of Silver Carp and environmental variables. Models built used combinations of the following environmental variables: cumulative reproductive season discharge (DISR), cumulative non-reproductive season discharge (DISNR), coefficient of variation in river discharge during the reproductive season

(COVR), annual degree days over 17°C (ADD), winter severity (WS), and summer severity (SS).

Variables were transformed to meet the assumptions of normality as needed. In order to distinguish the most parsimonious models, Akaike’s Information Criterion (AICc; AIC corrected for small sample size) and associated delta AICc (Δi) and Akaike weights (Wi) were used to rank models based on their relative support for the data. Models only with Δi values <2.0 and Wi values >0.1 were used for interpretation as they were considered to have the best support for the data.

To explore the effects of broad climatic conditions on Silver Carp recruitment patterns across the

Mississippi River watershed, age data taken from all sites were combined into a single age-frequency histogram and year-classes with less than five individuals present were omitted from the analysis.

Residuals (response variable) were calculated from the final catch-curve that included 2004-2009 year- classes. Next, year-class residuals were regressed against three large-scale environmental variables that could influence Silver Carp recruitment across a large geographic area: winter NAO averaged for the

November – February period for each year (data obtained from National Weather Service Climate 51

Prediction Center, College Park, MD, USA), winter ENSO averaged for the November – February period for each year (data obtained from National Weather Service Climate Prediction Center, College Park,

MD, USA), and the yearly averaged PHDI (data obtained from NOAA) for all states within the

Mississippi River watershed (excluding Louisiana and Mississippi). All statistical analysis were conducted in Program R Software Version 3.2.0 with a significance level of 0.05.

Results

In all, 871 Silver Carp were captured from nine Mississippi River watershed sites throughout the duration of this study. Based upon age-frequency distributions by study site (Figure 2), varying recruitment patterns were evident. RVI scores varied among sites (0.66 – 0.90); yet, scores were all greater than 0.5, indicating consistent recruitment (Figure 2). During 2006, populations from the middle

Mississippi River had a very weak year-class while populations from the lower Mississippi River had a stronger year-class (Figure 3). Silver Carp populations captured from the Des Moines River confluence,

Illinois River confluence, and both the lower and middle Mississippi River sites had stronger year-classes during 2007 whereas both Wabash River sites and the upper Illinois River sites exhibited weaker year- classes during 2007 (Figure 3). During 2009, Carp captured from both the Missouri and upper Illinois river sites exhibited stronger year-classes compared to other sites (Figure 3). Differing from most other sites, Silver Carp populations captured from both the lower and upper Wabash River sites exhibited strong year-classes during both 2005 and 2006 (Figure 3).

Correlation coefficients for the 21 bivariate combinations that were evaluated ranged from -1.0 to

0.85 (mean = -0.08; P-values <0.05 for three bivariate combinations; Figure 4). Ten (47.6%) correlation coefficients were greater than zero, indicating some degree of synchronous recruitment of Silver Carp populations between select sites. Alternatively, a greater proportion of correlations (52.4%) were negative, indicating asynchronous recruitment. Among all bivariate combinations, only three (14.2%) relationships were significant (P < 0.05), each including at least one Silver Carp population collected from the Wabash River. Silver Carp from the upper Wabash River site had high (r > 0.80) correlation 52

values for bivariate combinations with Carp populations captured from the lower Wabash River and the

Illinois River confluence site (both P < 0.05). Among bivariate combinations, Carp populations captured from the Des Moines, Illinois, and Wabash rivers consisted of either highly negative (ρ < -0.70) or positive (ρ > 0.70) correlations with other Silver Carp populations while populations captured from the middle and lower Mississippi River sites were moderately correlated or no correlation with other Silver

Carp populations captured throughout the Mississippi River watershed (mean ρ = 0.02 ± 0.12 SE; all P >

0.05).

Bivariate correlations of year-class strength were not possible for all locations, as Carp captured from the Missouri and middle Illinois Rivers commonly had fewer than three years of overlap in year- classes. Of the relationships evaluated, Silver Carp year-class strength from the Missouri River were highly correlated (ρ = 1.0) with Carp populations from the Upper Wabash River (linear distance between sites = 770 km). Silver Carp populations from the middle Illinois River were positively correlated with populations from the lower (ρ = 1.0) and middle Mississippi River (ρ = 1.0) and the lower Wabash River

(ρ = 0.50) and negatively correlated with Carp populations from the upper Illinois (ρ = -0.50) and upper

Wabash rivers (ρ = -0.50; linear distance between sites = 164.0 – 455.0 km).

Despite the amount of synchrony among some locations, Silver Carp recruitment was asynchronous across the Mississippi River watershed (t20 = -0.60, P = 0.72; Figure 4). According to the linear distance correlogram, mean correlation coefficients (± 95% CI) overlapped with zero or were negative (150-300 km; Figure 5), indicating that Silver Carp recruitment synchrony was unrelated to linear distance as expected. In contrast, river distance correlograms revealed that Silver Carp populations are synchronous up to 300 river km within the Mississippi River watershed as mean correlation coefficients (± 95% CI) were greater than zero (Figure 5). Mean correlation coefficients were less than zero for Silver Carp populations located 600 – 900 river km from one another (Figure 5), indicating synchronous recruitment at that spatial scale. Additionally, e-folding scale analyses for both linear and river mile distance were unable to converge due to the lack of synchrony exhibited at sites in close proximity. 53

Predictive models including metrics of river discharge (DISR, DISNR, or COVR) received more support for explaining inter-annual variation in Silver Carp recruitment than models including annual degree-days (ADD), summer severity (SS), and winter severity (WS; Table 2). The top three most parsimonious models included all three metrics of river discharge (0 < Δi < 2.0 and Wi > 0.1; Table 2).

The model receiving the most support included the cumulative coefficient of variation of the mean daily discharge for the reproductive season (COVR; AIC = -67.67, Wi = 0.41) followed by a model including cumulative river discharge during both the reproductive season (DISR; Δi = 1.27, Wi = 0.22) and non- reproductive season (DISNR; Δi = 1.30, Wi = 0.22). In most instances, cumulative river discharge during both the reproductive was positively (95% CI of slope: 0.003 ± 0.024) related to year-class strength and cumulative river discharge during the non-reproductive season was negatively (95% CI of slope: -0.005 ±

0.023) related to year-class strength, but relationships were variable among rivers (Figure 6). The cumulative coefficient of variation of the mean daily discharge for the reproductive season was negatively

(95% CI of slope: 0.002 ± 0.045) related to year-class strength (Figure 6). Of models receiving moderate support (2.0 < Δi < 6.0), summer severity (SS; Δi = 2.60, Wi = 0.11) as well as the additive effects of river discharge during both the reproductive and non-reproductive season (Δi = 5.88, Wi = 0.02) were included

(Table 2). All other models (n = 54) received substantially less support (Δi > 6.0).

Combined among all sites, Silver Carp throughout the Mississippi River basin had consistent recruitment (RVI = 0.66; Figure 7). Stronger year-classes were present during 2005 – 2008 (0.0 < residual values < 1.0) while weaker year-classes were present during both 2004 and 2009 (residual values equaled -0.06 and -0.09, respectively). However, NAO (r = 0.27, P = 0.28), ENSO (r = 0.05, P = 0.68), and PHDI (r = 0.23, P = 0.68) indices were not related to Silver Carp year-class strength (Figure 8).

Discussion

Contrary to my hypothesis, recruitment of Silver Carp populations inhabiting the Mississippi

River watershed during 2002-2010 was asynchronous across study sites (0-550 km), which is varying from reproductive habits of select ubiquitous freshwater fish populations inhabiting both lotic 54

(Grenouillet et al. 2001; Cattanéo et al. 2003) and lentic (Myers et al. 1997; Phelps et al. 2008;

Dembkowski et al. 2016; Honsey et al. 2016) systems. Moreover, the Moran effect has been evaluated for a variety of freshwater species, including Common Carp (Phelps et al. 2008), Yellow Perch

(Dembkowski et al. 2016; Honsey et al. 2016), Brown Trout (Cattanéo et al. 2003), Walleye (Sander vitreus; Koonce et al. 1977; Colby et al. 1979; Schupp 2002), Roach Rutilus rutilus (Grenouillet et al.

2001), and Lake Michigan planktivorous species (Bunnell et al. 2016), but had yet to be evaluated for a highly invasive, riverine species. Interestingly, regional climatic variables were not influential in regulating year-class strength of Silver Carp populations, suggesting a lack of the Moran effect across the multiple populations inhabiting the Mississippi River watershed. In contrast, Silver Carp year-class strength seemed to be influenced more by local environmental variables (indices of river discharge).

Despite expectations, Silver Carp recruitment into the adult population is consistent (indicated by

RVI scores) across the Mississippi River watershed. In their invaded range, Silver Carp recruitment has become limited due to anthropocentric alterations and disruption of the natural flow regime, resulting in population declines (Yi et al. 2010; Li et al. 2016). Within the Mississippi River watershed, Silver Carp reproduction has been documented in the Missouri (Schrank et al. 2001), Illinois (DeGrandchamp et al.

2007; Norman and Whitledge 2015), Mississippi (Lohmeyer and Garvey 2009), Des Moines (Camacho

2016), and Wabash (Coulter et al. 2013) rivers in a variety of years, indicating recruitment across a broad geographic scale. Also, Silver Carp populations often have erratic recruitment, as large-scale flood may stimulate stronger year-classes during individual years. For example, age structure of Silver Carp in three

Missouri River tributaries was dominated by the 2010 year-class that coincide with a large flood event

(Hayer et al. 2014). Similarly, Asian Carp populations in the middle Mississippi River and the Illinois

River confluence were composed mainly by the 2000 year-class that also occurred during large-scale flooding (Garvey et al. 2006). Although Silver Carp year-class strength was influenced by metrics of river discharge, it was also generally consistent across sites. Thus, although increases in discharge can promote year-class success, Silver Carp reproduction is plastic and recruitment can be successful under a wide range of environmental conditions. 55

Although synchronous recruitment of freshwater fishes can extend to spatial scales > 50 km (e.g.,

Phelps et al. 2008; Myers et al. 2015; Honsey et al. 2016), the results herein indicate that Silver Carp recruitment does not exhibit synchronous fluctuations. As such, the current analysis provides insight into the importance of local-scale environmental factors rather than regional-scale factors on Silver Carp recruitment. Two explanations could help elucidate the lack of synchrony among populations. First, the spatial extent of synchrony generally occurs at distances less than 50 km for a suite of freshwater fish species, and even at distances less than 15 km in some instances (e.g., Northern Pike Esox lucius; Myers et al. 1997). Within the current study, the shortest distance between sites able to be analyzed for synchrony was 75.4 km (lower and middle Mississippi River sites). Hence the lack of sites located closer in proximity could have led to a lack of synchrony at small spatial scales. Alternatively, the hydrographs of the major Mississippi River tributaries analyzed in this study fluctuate asynchronously, causing asynchronous fluctuations in Silver Carp recruitment. For example, Silver Carp in the Des Moines River experienced a strong year-class during 2007 in response to a long-term flood event during the reproductive season whereas populations from the Illinois River experienced a weak year class in response to low-flow conditions present during the reproductive season. Similarly, Brown Trout populations inhabiting French rivers did not display recruitment synchrony across 57 sites as hydrology differently affected subpopulations (site distances approximately 10 – 1,000 km; Cattanéo et al. 2003).

Thus, the variation in localized environmental conditions is likely an important factor regulating Silver

Carp recruitment at small spatial scales resulting is asynchronous recruitment.

Of the local environmental variables included in the analysis, models including metrics of river discharge received the most support in explaining the observed variability in recruitment of Silver Carp populations across the Mississippi River watershed. Despite relatively consistent recruitment among populations, patterns of high, sustained discharge events during both the reproductive and non- reproductive seasons typically led to relatively stronger year-classes of Silver Carp while variation in river discharge during the reproductive season was negatively related to year-class strength. For example, 56

Silver Carp populations captured from the middle and upper Illinois River sites produced stronger year- classes during 2009 where high, sustained discharge events were present for greater than three months

(USGS 2016). Similarly, Silver Carp populations captured in the middle Mississippi River as well as at the Illinois River confluence displayed similar patterns as stronger year-classes were produced during

2008. Across studies, similar patterns have been qualitatively discussed, as strong year-classes were produced in years with extreme increases in river discharge (Hayer et al. 2014) as well as the combination of high discharge and temperatures are above 17°C in the UMR (Schrank and Guy 2002; Garvey et al.

2006; DeGrandchamp et al. 2007; Lohmeyer and Garvey 2009), but had yet been evaluated across multiple sites. Similarly, high water levels also result in large year-classes of fishes in lentic systems

(Phelps et al. 2008; Dembkowski et al. 2016), potentially augmenting productivity, inundating larval fish nursery habitat, provide spawning substrate, and provide predator refuge habitat (Nunn et al. 2012).

Given the stochastic nature of lotic systems, the availability of nursery habitat becomes crucial to young- of-year fish survival. Spawning during high flow can facilitate larval dispersal downriver to floodplain, creek, or channel habitats that serve as nursey areas, increasing larval survival (Nikolsky 1963; Huet

1970). Alternatively, low flow conditions have the ability to disconnect mainstem habitats from nursery habitats, influencing year-class strength. Interestingly, year-classes of Silver Carp populations inhabiting both of the Wabash River seem to be less reliant upon flood events to produce strong year-classes, potentially due to the free-flowing nature of the Wabash River and the decreased reliance on dam operations to provide adequate spawning discharges and access to critical nursery habitat. Collectively, elevated, sustained river discharge during the first year of life seems to be influential in regulating year- class strength of Silver Carp at local scales across the Mississippi River watershed.

Large-scale recruitment in freshwater fishes is often synchronous across broad geographic areas in response to similarities in temperature regimes. For example, Roach recruitment in the Rhône River was highly synchronous over a 10 year period in response to June water temperatures (Grenouillet et al.

2001). Although there was a lack of significance at both the local- and regional-scale, the influence of 57

summer air temperatures (via NAO and moderate importance of SS) on Silver Carp year-class strength underscores the importance of temperature during early life stages. Silver Carp egg embryo’s and larvae tend to develop faster at warmer temperatures (Chapman and George 2011) and accelerated early-life ontogenetic diet shifts due to quicker development can lead to a longer exogenous feeding period and improved swimming ability, increasing overall growth during the first year of life. In contrast, summer temperatures exceeding an upper thermal tolerances (27°C; Kolar et al. 2007) may decrease growth rates, as a greater amount of resources are required for maintenance rather than tissue growth (e.g., Eldridge et al. 2015). Subsequently, year-class success was hypothesized to increase in response elevated temperatures throughout the first growing season (Chapman and George 2011). Silver Carp year-class strength within the Mississippi River watershed tended to be positively related to summer severity

(moderate model support) and annual degree days over 17°C. Silver Carp larvae tend to seek out shallow backwater nursery habitats throughout the summer and elevated temperatures that may lead to faster growth rates, quicker shifts to exogenous feeding larvae, and increased swimming ability (George and

Chapman 2013). As such, elevated summer temperatures seem to only moderately promote Silver Carp year-class strength, and can potentially work in conjunction with high river discharge events. Combined,

Silver Carp populations across the Mississippi River watershed experience stronger year-classes during periods of elevated temperature regimes.

The effects of dispersal on recruitment of river fishes have been accounted for through sampling site selection (e.g., spatial segregation by diversion dams; Grenouillet et al. 2001) or ensuring that sites are isolated from one another (e.g., Tedesco et al. 2004). In this study, there is a lack of physical barriers that inhibit longitudinal movements, allowing Silver Carp to freely move among sites. Thus, it is difficult to separate the potential effects of dispersal versus similarities in environmental conditions that can cause synchronous recruitment of Silver Carp at varying spatial scales. Importantly, a relative rudimentary assumption of fish dispersal is that individual dispersal is uniform to all available habitats or locations

(i.e., equal proportion of fish to each available location) and likely consistent (see details in Ripa 2000; 58

Goldwyn and Hastings 2011). In practice, fish dispersal may instead be dependent upon prevailing abiotic and biotic conditions and would perhaps be stochastic, not chaotic, in nature and such patterns have been exhibited in Silver Carp movement patterns with both the Wabash (Coulter et al. 2016) and

Illinois (Norman and Whitledge 2015; DeGrandchamp et al. 2016) rivers. Silver Carp recruitment was synchronous at <300 river km but was not synchronous at any linear distance spatial scale, suggesting dispersal may influence recruitment synchrony on small spatial scales. However, this result is based on a limited number of observations (n=3) and abiotic factors appear to have a larger effect on asynchronous recruitment patterns at larger spatial scales.

The information provided herein will lead to an improved understanding of Silver Carp recruitment dynamics throughout North America and represents a positive step towards understanding the underlying mechanisms influencing recruitment by identifying important environmental variables associated with successful reproduction. In addition, these results may be applicable for multiple Asian

Carp species inhabiting the Mississippi River watershed. Currently, the Mississippi River has reproducing populations of Bighead (i.e., Schrank et al 2001), Grass (Raibley et al. 1995), and Black

(Associated Press 2016) carp, all posing a severe threat to native biodiversity throughout the watershed.

As Bighead (Kolar et al. 2007), Grass (Stanley et al. 1978), and Black (Banarescu and Coad 1993) carp all have similar reproductive requirements, the results presented herein can be broadly applied to individual species for forecasting strong or weak year-classes and potential population trajectories.

Literature Cited

Abdusamadov AS (1987) Biology of White Amur, Ctenopharyngodon idella, Silver Carp, Hypophthalmichthys molitrix, and Bighead, Aristichthys nobilis, acclimatized in the Terek region of the Caspian Basin. Journal of Ichthyology 26:41-49

Adams SM, McLean RB, Huffman MM (1982) Structuring of a predator population through temperature- mediated effects on prey availability. Canadian Journal of Fisheries and Aquatic Sciences 39:1175-1184

Associated Press (2016) Scientists: Discovery of young, wild Black Carp troubling. Southeast Missourian, 07 Mar. 2016. Web. 26 Oct. 2016 Banarescu P, Coad BW (1993) Cyprinids of Eirasia. Pages 127-155 in: I.J. Winfield and J.S. Nelson (eds). Cyprinid fishes: Systematics, biology and exploitation. Chapman and Hall, New York Bunnel DB, Adams JV, Gorman OT, Madenjian CP, Riley SC, Roseman EF, Shaeffer JS (2010) Population synchrony of a native fish across three Laurentian Great Lakes: evaluating the effects of dispersal and climate. Oecologia 162:641-651 Bunnell DB, Höök TO, Troy CD, Liu W, Madenjian CP, Adams JV (2016) Testing for synchrony in recruitment among four Lake Michigan fish species. Canadian Journal of Fisheries and Aquatic Sciences. DOI: 10.1139/cjfas-2015-0534 Cattanéo F, Hugueny B, Lamouroux N (2003) Synchrony in Brown Trout, Salmo trutta, population dynamics: a ‘Moran effect’ on early-life stages. OIKOS 100:43-54 Chang WYB (1966) Culture of freshwater fish in Chine. In E.o> Gangstad, editor. 1980. Chinese fish culture. Report 1. Technical report A-79. Aquatic plant control research program. Washington, D.C. U.S. Army Waterways Experiment Station (draft translated by Koo TSY, 1980) Chapman DC, George AE (2011) Developmental rate and behavior of early life stages of Bighead Carp and Silver Carp. U.S. Geological Survey Scientific Investigations Report 2011-5076, 11p Chezik KA, Lester NP, Venturelli PA (2014a) Fish growth and degree-days I: selecting a base temperature for a within population study. Canadian Journal of Fisheries and Aquatic Sciences 71:47-55 Chezik KA, Lester NP, Venturelli PA (2014b) Fish growth and degree-days II: selecting a base temperature for an among population study. Canadian Journal of Fisheries and Aquatic Sciences 71:1-9 Colby PJ, McNichol RE, Ryder RA (1979) Synopsis of biological data on the Walleye Stizostedion vitreum (Mitchill 1818). Food and Agricultural Organization of the United Nations Fisheries Synopsis no. 119, Rome, Italy Coulter AA, Keller D, Amberg JJ, Bailey EJ, Goforth RR (2013) Phenotypic plasticity in the spawning traits of Bigheaded Carp (Hypophthalmichthys spp.) in novel ecosystems. Freshwater Biology 57:1029-1037 Coulter AA, Bailey EJ, Keller D, Goforth RR (2016) Invasive Silver Carp movement patterns in the predominantly free-flowing Wabash River (Indiana, USA). Biological Invasions 18:471-485 DeGrandchamp KL, Garvey JE, Csoboth LA (2007) Linking adult reproduction and larval density of invasive Carp in a large river. Transactions of the American Fisheries Society 136:1327-1334 60

DeGrandchamp KL, Garvey JE, Colombo RE (2008) Movement and habitat selection by invasive Asian Carps in a large river. Transactions of the American Fisheries Society 137:45-56 Dembkowski DJ, Willis DW, Wuellner MR (2016) Synchrony in larval Yellow Perch abundance: the influence of the Moran Effect during early life history. Canadian Journal of Fisheries and Aquatic Sciences. DOI: 10.1139/cjfas-2015-0310 Deters JE, Chapman DC, McElroy B (2013) Location and timing of Asian Carp spawning in the lower Missouri River. Environmental Biology of Fishes 96:617-629 Dettmers JM, Raffenberg MJ, Weis AK (2003) Exploring zooplankton changes in southern Lake Michigan: implications for Yellow Perch recruitment. Journal of Great Lakes Research 29:355- 364 Eldridge WH, Sweeney BW, Law JM (2015) Fish growth, physiological stress, and tissue condition in response to rate of temperature change during cool or warm diel thermal cycles. Canadian Journal of Fisheries and Aquatic Sciences 72:1527-1537 Freeze M, Henderson S (1982) Distribution and status of the Bighead Carp and Silver Carp in Arkansas. North American Journal of Fisheries Management 2:197-200 Garvey JE, DeGrandchamp KL, Williamson CJ (2006) Life history attributes of Asian Carps in the upper Mississippi River system. Reports. Paper 3. http://opensiuc.lib.siu.edu/fiaq_reports/3 George AE, Chapman DC (2013) Aspects of embryonic and larval development in Bighead Carp Hypophthalmichthys nobilis and Silver Carp Hypophthalmichthys molitrix. PLoS ONE 8:e73829. doi:10.1371/journal.pone.0073829 Goldwyn EE, Hastings A (2011) The roles of the Moran effect and dispersal in synchronizing oscillating populations. Journal of Theoretical Biology 289:237-246 Grenouillet G, Hugueny B, Carrel GA, Olivier JM, Pont D (2001) Large-scale synchrony and inter-annual variability in Roach recruitment in the Rhone River: the relative role of climate factors and density-dependent processes. Freshwater Biology 46:11-26 Guy CS, Willis DW (1995) Population characteristics of Black Crappie in South Dakota waters: a case for ecosystem-specific management. North American Journal of Fisheries Management 15:754- 765 Haydon D, Steen H (1997) The effects of large- and small-scale random events on the synchrony of metapopulation dynamics: a theoretical analysis. Proceedings of the Royal Society B 264:1375- 1381 Hayer CA, Breeggemann JJ, Klumb RA, Graeb BD, Bertrand KN (2014) Population characteristics of Bighead and Silver Carp on the northwestern front of their North American invasion. Aquatic Invasions 9:289-303 Heim RR (2002) A review of twentieth-century drought indices used in the United States. Bulletin of the American Meteorological Society 83:1149-1165 Henderson PA, Corps M (1997) The role of temperature and cannibalism in interannual recruitment variation of bass in British waters. Journal of Fish Biology 50:280-295 Hjort J (1926) Fluctuations in the year classes of important food fishes. ICES Journal of Marine Science 1:5-38 61

Honsey AE, Brunnel DB, Troy CD, Fielder DG, Thomas MV, Knight CT, Chong SC, Höök TO (2016) Recruitment synchrony of Yellow Perch (Perca flavescens, Percidae) in the Great Lakes regions, 1966-2008. Fisheries Research 181:214-221 Huet M (1970) Textbook of fish culture: breeding and cultivation of fish. Fishing News Ltd., Surrey and London Hurrell JW (1995) Decadal trends in the North Atlantic oscillation regional temperatures and precipitation. Science 269:676-679 Irons KS, Sass GG, McClelland MA, Stafford JD (2007) Reduced condition factor of two native fish species coincident with invasion of nonnative Asian Carps in the Illinois River, U.S.A. Is this evidence for competition and reduced fitness? Journal of Fish Biology 71:258-273 Janáč M, Ondračková M, Jurajda P, Valová Z, Reichard M (2010) Flood duration determines the reproduction success of fish in artificial oxbows in a floodplain of a potamal river. Ecology of Freshwater Fish 19:644-655 Junk WJ, Bayley PB, Sparks RE (1989) The flood pulse concept in river-floodplain systems. Proceedings of the International Large River Symposium. Canadian Special Publications in Fisheries and Aquatic Sciences 106:110-127 Kaul M, Rishi KK (1993) Exotic Chinese Carps. Punjab Fisheries Bulletin 27:53-56 Kendall BE, Bjørnstad ON, Bascompte J, Keitt TH, Fagan WF (2000) Dispersal, environmental correlation, and spatial synchrony in population dynamics. The American Naturalist 155:628-636 Kocovsky PM, Chapman DC, McKenna JE (2012) Thermal and hydrological suitability of Lake Erie and its major tributaries for spawning of Asian Carps. Journal of Great Lakes Research 38:159-166 Koenig WD (1999) Spatial autocorrelation of ecological phenomena. TREE 14: 22-26 Koenig WD, Knops JM (1998) Testing for spatial autocorrelation in ecological studies. Ecography 21:423-429 Kolar CS, Chapman DC, Courtenay WR, Housel CM, Williams JD, Jennings DP (2007) Bigheaded Carps: a biological synopsis and environmental risk assessment. Special Publication 33. American Fisheries Society, Bethesda, Maryland Koonce JF, Bagenal TB, Carline RF, Hokanson KEF, Nagięć M (1977) Factors influencing year-class strength of percids: a summary and model of temperature effects. Journal of Fisheries Research Board of Canada 34:1900-1909 Krykhtin ML, Gorbach EI (1981) Reproductive ecology of the Grass Carp, Ctenopharyngodon idella, and the Silver Carp, Hypophthalmichthys molitrix, in the Amur Basin. Journal of Ichthyology 21:109- 123 Lande R, Engen S, Sæther BE (1999) Spatial scale of population synchrony: Environmental correlation versus dispersal and density regulation. The American Naturalist 154:271-279 Li C, Peng J, Liao W (2006) Study on the eco-hydrological factors and flow regime requirements on spawning of four major Chinese Carps in the middle reaches of the Yangtze River. Journal of China Institute of Water Resources and Hydropower Research 14:170-176 62

Li M, Duan Z, Gao X, Cao W, Liu H (2016) Impact of the Three Gorges Dam on reproduction of four major Chinese Carp species in the middle reaches of the Changjiang River. Chinese Journal of Oceanology and Limnology 34:885-893 Lohmeyer AM, Garvey JE (2009) Placing the North American invasion of Asian Carp in a spatially explicit context. Biological Invasions 11:905-916 Maceina MJ (1997) Simple application of using residuals from catch-curve regressions to assess year- class strength in fish. Fisheries Research 32:115-121 Madeira D, Araújo JE, Vitorino R, Capelo JL, Vinagre C, Diniz MS (2016) Ocean warming alters cellular metabolism and induces mortality in fish early life stages: A proteomic approach. Environmental Research 148:164-176 McClelland MA, Sass GG (2008) The long-term Illinois River fish population monitoring program. Illinois Natural History Survey, Technical Report Miyazono S, Aycock JN, Miranda LE, Tietjen TE (2010) Assemblage patterns of fish functional groups relative to habitat connectivity and conditions in floodplain lakes. Ecology of Freshwater Fish 19:578-585 Moran PA (1953) The statistical analysis of the Canadian Lynx cycle, II. Synchronization and Meteorology. Australian Journal of Zoology 1:291-298 Myers RA, Mertz G, Bridson J (1997) Spatial scales of interannual recruitment variations of marine, anadromous, and freshwater fish. Canadian Journal of Fisheries and Aquatic Sciences 54:1400- 1407 Myers JT, Yule DL, Jones ML, Ahrenstorff TD, Hrabik TR, Claramunt RM, Ebener MP, Berglund EK (2015) Spatial synchrony in Cisco recruitment. Fisheries Research 165: 11-21 Nico LG, Williams JD, Jelks HL (2005) Black carp: biological synopsis and rish assessment of an introduced fish. American Fisheries Society Special Publication 31, Bethesda, Maryland Nikolsky GV (1963) The ecology of fishes. Academic Press, London and New York Norman JD, Whitledge GW (2015) Recruitment sources of invasive Bighead Carp (Hypopthalmichthys nobilis) and Silver Carp (H. molitrix) inhabiting the Illinois River. Biological Invasions 17:2999- 3014 Nunn AD, Tewson LH, Cowx IG (2012) The foraging ecology of larval and juvenile fishes. Reviews in Fish Biology and Fisheries 22:377-408 Oden NL, Sokal RR (1986) Directional autocorrelation: An extension of spatial correlograms to two dimensions. Systematic Biology 35:608-617 Papoulias DM, Chapman D, Tillitt DE (2006) Reproductive condition and occurrence of intersex in Bighead and Silver Carp in the Missouri River. Hydrobiologia 571:355-360 Phelps QE, Graeb BD, Willis DW (2008) Influence of the Moran Effect on spatiotemporal synchrony in Common Carp recruitment. Transactions of the American Fisheries Society 137:1701-1708 Pyper BJ, Mueter FJ, Peterman RM, Blackbourn DJ, Wood CC (2001) Spatial covariation in survival rates of Northeast Pacific Pink Salmon (Oncorhynchus gorbuscha). Canadian Journal of Fisheries and Aquatic Sciences 58:1501-1515 63

Raibley PT, Blodgett D, Sparks RE (1995) Evidence of Grass Carp (Ctenopharyngodon idella) reproduction in the Illinois and Upper Mississippi Rivers. Journal of Freshwater Ecology 10:65- 74 Ranta E, Kaitala V, Lindström J (1998) Spatial dynamics of populations: In: Modeling Spatiotemporal Dynamics in Ecology. Eds. J Bascompte and R.V. Solé, Springer, Berlin. 47-62pp Ripa J (2000) Analysing the Moran effect and dispersal: their significance and interaction in synchronous population dynamics. Oikos 90:175-187 Ruiz GM, Fofonoff P, Hines AH, Grosholz ED (1999) Non-indigenous species as stressors in estuarine and marine communities: assessing invasion impacts and interactions. Limnology and Oceanography 44:950-972 Sass GG, Cook TR, Irons KS, McClelland MA, Michaels NN, O’Hara TM, Stroud MR (2010) A mark- recapture population estimate for invasive Silver Carp (Hypophthalmichthys molitrix) in the La Grange Reach, Illinois River. Biological Invasions 12:433-436 Schrank SJ, Braaten PJ, Guy CS (2001) Spatiotemporal variation in density of larval Bighead Carp in the lower Missouri River. Transactions of the American Fisheries Society 130:809-814 Schrank SJ, Guy CS (2002) Age, growth, and gonadal characteristics of adult Bighead Carp, Hypophthalmichthys nobilis, in the lower Missouri River. Environmental Biology of Fishes 64:443-450 Schupp DH (2002) What does Mt. Pinatubo have to do with Walleyes? North American Journal of Fisheries Management 22:1014-1020 Seibert JR, Phelps QE (2013) Evaluation of Aging Structures for Silver Carp from Midwestern U.S. Rivers. North American Journal of Fisheries Management 33:839-844 Stanley JG, Miley II WW, Sutton DL (1978) Reproductive requirements and likelihood for naturalization of escaped Grass Carp in the United States. Transactions of the American Fisheries Society 107:119-128 Stuck JG, Porreca AP, Wahl DH, Colombo RE (2015) Contrasting population demographics of Invasive Silver Carp between an impounded and free-flowing river. North American Journal of Fisheries Management 35:114-122 Tedesco PA, Huegeny B, Paugy D, Fermon Y (2004) Spatial synchrony in population dynamics of West African fishes: a demonstration of an intraspecific and interspecific Moran effect. Journal of Animal Ecology 73: 693-705 Titus RG, Mosegaard H (1992) Fluctuating recruitment and variable life history of migratory Brown Trout, Salmo trutta L., in a small, unstable stream. Journal of Fish Biology 41:239-255 U.S. Geological Survey (2016) October. USGS water resources of the United States. http://nwis.waterdata.usgs.gov/usa/nwis/uv/?cb_00055=onandcb_00060=onandcb_00065=onandf ormat=gif_statsandsite_no=05568500andperiod=andbegin_date=2009-01-01andend_date=2009- 12-31 Verigin BV, Makeyeva AP, Zaki Mokhamed MI (1978) Natural spawning of the Silver Carp (Hypophthalmichthys nobilis), the Bighead Carp (Aristichthys nobilis), and the Grass Carp (Ctenopharyngodon idella) in the Syr-Dar’ya River. Journal of Ichthyology 18:143-146 64

Wang S, Liao W, Chen D, Duan X, Peng Q, Wang K, Li C (2008) Analysis of eco-hydrological characteristics of the four Chinese farmed Carps’ spawning grounds in the middle reach of the Yangtze River. Resources and Environmental in the Yangzte Basin 17:892-897 Wanner GA, Klumb RA (2009) Asian Carp in the Missouri River: Analysis from multiple Missouri River habitat and fisheries programs. National Invasive Species Council materials. Paper 10 National Invasive Species Council materials. Paper 10 Williamson CJ, Garvey JE (2005) Growth, fecundity, and diets of newly established Silver Carp in the middle Mississippi River. Transactions of the American Fisheries Society 134:1423-1430 Yi B, Yu Z, Liang Z, Sujuan S, Xu Y, Chen J, He M, Liu Y, Hu Y, Deng Z, Huang S, Sun J, Liu R, Xiang Y (1988) The distribution, natural conditions, and breeding production of the spawning ground on main stream of Yangtze River. In: Yi B, Yu Z, Liang Z (eds) Gezhouba water control project and four famous fishes in the Yangtze River. Hubrei Science and Technology Press, Wuhan:1-46 Yi Y, Wang Z, Yang Z (2010) Impact of the Gezhouba and Three Gorges Dams on habitat suitability of carps in the Yangtze River. Journal of Hydrology 387:283-291 Zhang G, Chang J, Shu G (2000) Application of factor-criteria system reconstruction analysis in the reproduction research on Grass Carp, Black Carp, Silver Carp, and Bighead in the Yangtze River. International Journal of General Systems 29:419-428 Zhang Y, Wallace JM, Battisti DS (1997) ENSO-like interdecadal variability: 1900-93. Journal of Climate 10: 1004-1020 Zhou Q, Xie P, Xu J, Ke Z, Guo L (2009) Growth and food availability of Silver and Bighead Carps: evidence from stable isotope and gut content analysis. Aquaculture Research 40:1616-1625 Zorn TG, Nuhfer AJ (2007) Regional synchrony of Brown Trout and Brook Trout population dynamics among Michigan rivers. Transactions of the American Fisheries Society 136:706-717

Tables and Figures

Table 1. Reference number, latitude, and longitude of each of the nine Mississippi River watershed sampling sites used to assess regional synchrony of Silver Carp.

Site Reference Number Latitude Longitude Missouri River 1 41°36'19.47"N 96° 6'51.99"W Des Moines River Confluence 2 40°23'35.60"N 91°22'9.49"W Upper Illinois River 3 41°19'38.08"N 89° 0'35.42"W Middle Illinois River 4 40° 9'47.84"N 90°12'22.66"W Illinois River Confluence 5 38°55'59.71"N 90°16'39.59"W Middle Mississippi River 6 37°15'8.88"N 89°30'48.76"W Lower Mississippi River 7 36°34'41.74"N 89°29'58.12"W Lower Wabash River 8 38° 7'51.05"N 87°56'34.39"W Upper Wabash River 9 39° 6'36.07"N 87°39'18.00"W

Table 2. Model rankings evaluating Silver Carp recruitment in the Mississippi River watershed.

Variables included were log-transformed cumulative coefficients of variation in river discharge (m3/s) during the reproductive season (May-June; COVR), log-transformed cumulative river discharge (m3/s) during the reproductive season (DISR) and the non-reproductive season (June-October; DISNR), cumulative annual degree-days over 17°C (ADD), cumulative annual degree days over 27°C (summer severity; SS), and cumulative annual degree days under 0°C (winter severity; WS). Other abbreviations are as follows: K = the number of parameters estimated, AICc = Akaike’s information criterion, Δi = the difference between the AIC value of the most parsimonious model and model i, and Wi = the relative support for model i.

Model K AICc Δi Wi COVR 3 -67.66 0.00 0.41 DISR 3 -66.39 1.27 0.22 DISNR 3 -66.37 1.30 0.21 SS 3 -65.06 2.60 0.11 DISR + DISNR 4 -61.79 5.88 0.02 DISR + COVR 4 -60.40 7.27 0.01 DISNR + COVR 4 -60.14 7.52 0.01 COVR + SS 4 -58.47 9.19 0.00 DISR + SS 4 -57.11 10.55 0.00 DISNR + SS 4 -57.08 10.59 0.00 DISR + DISNR + COVR 5 -55.89 11.77 0.00 WS 3 -54.90 12.76 0.00 DISR + DISNR + SS 5 -52.41 15.26 0.00 DISR + COVR + SS 5 -51.32 16.35 0.00 ADD + SS 3 -51.97 15.69 0.00 DISNR + COVR + SS 5 -50.96 16.70 0.00 DISR + DISNR + COVR + SS 5 -50.96 16.70 0.00 COVR + WS 4 -48.86 18.81 0.00 DISNR + WS 4 -47.20 20.46 0.00 DISR + WS 4 -47.17 20.49 0.00

Figure 1. Location of the nine Mississippi River watershed sampling sites used to assess regional synchrony of Silver Carp (See Table 1 for site names and associated reference number [1 – 9] and coordinates). 68

Figure 2. Silver Carp year-class histogram and associated RVI scores from nine locations across the

Mississippi River watershed.

Figure 3. Spatiotemporal trends in Silver Carp year-class strength (residual values) collected from nine sites located throughout the Mississippi River watershed. Residual values are indicative of relative year- class strength as positive values denote strong year-classes and negative values denote weak year-classes. 70

Figure 4. Pairwise Spearman’s rank correlation coefficients (ρ) of year-class strength among Mississippi

River Silver Carp populations. The black vertical line represents the expected correlation given asynchronous recruitment patterns, and the dashed vertical line represents the mean ρ across all bivariate comparisons.

Figure 5. Linear distance (top) and river distance (bottom) versus pairwise Spearman’s correlation coefficients (ρ) of relative year-class strength among Mississippi River Silver Carp populations. Black triangles represent mean ρ (± 95% CI) values for individual distance categories. 72

Figure 6. Log-transformed studentized residuals from catch-curve regressions (Z axis) and significant environmental variables (columns; Y axis) included in the most parsimonious models evaluating the influence of environmental variables on Mississippi River Silver Carp populations by year-class (X axis).

The variables included were log-transformed cumulative coefficients of variation in river discharge (m3/s) during the reproductive season (May-June; COVR), log-transformed cumulative river discharge

(m3/s/1000) during the reproductive season (DISR), and log-transformed cumulative river discharge

(m3/s/1000) during the non-reproductive season (June-October; DISNR).

Figure 7. Silver Carp year-class frequency histogram for all fish captured throughout the Mississippi

River watershed during 2015 and associated RVI score. 75

Figure 8. Annual North Atlantic Oscillation Index (NAO; top figure), El Niño Southern Oscillation Index

(ENSO; middle), and Palmer Hydrological Drought Index (PHDI; bottom) indices regressed against studentized residuals from catch-curve regressions (year-class strength; Y axis) evaluating the Moran effect on recruitment of Silver Carp in the Mississippi River watershed. 76

CHAPTER 4. GENERAL CONCLUSIONS

Summary

Fisheries communities worldwide are becoming more uniform through the introduction and establishment of non-native species into novel habitats (Rahel 2002). The successful invasion of Silver

Carp into the Mississippi River watershed has become one of the more widely recognized introductions.

Efforts to gain an understanding of spatio-temporal fluctuations in Silver Carp populations at local- and regional-scales have been wide-reaching and are continually seeking to improve management and monitoring protocols. My study contributed to these efforts by 1) identifying intra-annual fluctuations in

Silver Carp population characteristics in a large river system where Carp have been present since the early

1990s and 2) evaluating local and regional abiotic factors that aid in determining year-class strength of

Silver Carp populations across the Mississippi River watershed.

My study evaluating intra-annual fluctuations in Silver Carp populations identified temporal patterns in population fluctuations that will be of interest to managers across the Mississippi River watershed. First, boat electroshocking catch rates exhibited a bimodal distribution, with peak capture rates occurring in late-spring and mid-fall and lower in summer during periods of high water temperature.

Interestingly, river discharge was positively related to catch rates only at upstream sites and the strength of the correlation decreased downstream. Silver Carp size structure was similar among months and sites except Silver Carp captured at Cliffland were smaller during the fall compared to earlier in the year. Last,

Silver Carp relative weight generally peaked during late spring and decreased throughout the year, indicative of a spring spawning fish. My results suggest that sampling of Silver Carp using electroshocking in late-spring (May-June) and fall (September-October) results in higher catch rates compared to summer sampling and a representative size structure. Thus, monitoring protocols should establish standardized sampling programs where sampling occurs during these periods of high densities in order to manage the spread and impacts of Silver Carp at state- and region-wide scales. 77

My study evaluating local and regional abiotic factors influencing Silver Carp year-class strength across the Mississippi River watershed found that populations are asynchronous and abiotic factors influence Carp populations at local scales. In all, Silver Carp populations are asynchronous (mean ρ = -

0.08 ± 0.13 SE) across the Mississippi River watershed while Mantel tests revealed that there was limited effect of dispersal or the Moran effect at the scale of the study. Populations <300 river km apart were synchronous, suggesting potential dispersal at local scales. In terms of local environmental factors influencing Silver Carp year-class strength, recruitment was negatively related to variability in river discharge (6 of 9 populations) and positively related to cumulative river discharge (7 of 9 populations) during the reproductive season, indicating that extended periods of elevated discharge are important local environmental factors regulating recruitment. Regionally, Silver Carp recruitment was not significantly related to the North Atlantic Oscillation Index (NAO), El Niño Southern Oscillation Index (ENSO), or

Palmer Hydrological Drought Index (PHDI), indicating that local-environmental factors have more influence on Silver Carp year-class strength than broad climatic conditions. In all, Silver Carp populations across the Mississippi River watershed exhibited asynchronous recruitment as local environmental factors influenced recruitment. Understanding recruitment dynamics of a highly invasive species throughout its range can aid managers in determining how populations will respond to both local and regional environmental conditions, aiding in determining future population trajectories.

Monitoring Silver Carp population characteristics and the abiotic factors influencing them can provide valuable knowledge to managers as natural resource agencies recognize the importance and necessity of collecting basic Asian Carp population information and its value in monitoring the spread and management of these populations (Conover and Simmonds 2007). In addition, the threat Asian Carp pose to currently uninvaded systems (e.g., the Great Lakes) and species (e.g., Paddlefish Polyodon spathula; Schrank et al. 2003) is immense and can have severe economic and ecological consequences

(Kolar et al. 2007). Hence, research evaluating methodological approaches to improve Carp capture or understand important environmental factors regulating recruitment is of critical importance. My research 78

has provided a time frame where Asian Carp capture rates are highest which will allow managers to conduct surveys with greater success and more accurate interpretation of their results. Silver Carp management also requires the knowledge of influential environmental factors regulating recruitment. I have provided information detailing the influence of local-scale environmental factors on inducing stronger year-classes of Silver Carp. Future research should investigate how density-dependent interactions as well as extreme environmental conditions (i.e., droughts, short summer periods, water quality parameters) influence Silver Carp reproductive success locally-and regionally.

Literature Cited

Rahel FJ (2002) Homogenization of freshwater fauna. Annual Review of Ecology and Systematics 33:291-315

Schrank SJ, Guy CS, Fairchild JF (2003) Competitive interactions between age-0 Bighead Carp and Paddlefish. Transactions of the American Fisheries Society 132:1222-1228

APPENDIX A

BIGHEAD CARP ELECTROSHOCKING CATCH-PER-UNIT-EFFORT (CPUE; MEAN

± SE) BY SAMPLING LOCATION AND MONTH DURING 2014 AND 2015.

Site April May June July August September October 2014 Eddyville 0 0 0 0 0 0 0 Cliffland 0 0 0 0 0 0 12.8±8.2 Keosauqua 0 1.3±1.3 0 0 0 1.3±1.3 0 Keokuk 1.3±1.3 1.3±1.3 0 0 0 0 2.3±2.3 2015 Eddyville 0 0 0 1.2±1.1 0 1.3±1.2 0 Cliffland 3.5±1.0 5.3±2.3 4.0±2.0 0 1.3±1.2 0 1.3±1.2 Keosauqua 1.3±1.2 0 0 0 0 0 NA Keokuk 2.7±0.8 9.6±1.1 2.4±0.8 0 0 1.2±1.1 0

APPENDIX B

BIGHEAD CARP LENGTH-FREQUENCY DISTRIBUTIONS AND PROPORTIONAL SIZE DISTRIBUTION (PSD; P – PREFERRED, M – MEMORABLE, T – TROPHY) INDICES DURING 2014 AND 2015 FROM ELECTROSHOCKING AND TRAMMEL NETS FROM FOUR SITES WITHIN THE DES MOINES RIVER, USA. N = NUMBER OF BIGHEAD CARP CAPTURED AT EACH SITE.

APPENDIX C

BIGHEAD CARP Wr (MEAN ± SE) BY SAMPLING MONTH COLLECTED AT

EDDYVILLE, CLIFFLAND, KEOSAUQUA, AND KEOKUK DURING 2014 AND 2015.

Site April May June July August September October Eddyville NA 101 ± 1 NA 94 NA 82 NA Cliffland 110 ± 2 110 94 ± 2 83 ± 4 84 87 ± 3 94 ± 7 Keosauqua 119 92 NA NA NA 91 NA Keokuk 116 ± 3 95 ± 3 88 ± 3 89 ± 5 NA 87 ± 7 98 ± 1

APPENDIX D

LEAST SQUARE REGRESSION ANALYSIS AND ASSOCIATED SPEARMAN’S RANK

CORRELATION COEFFICIENT (ρ) OBTAINED WHEN REGRESSING RESIDUAL VALUES

OBTAINED FOR SILVER CARP POPULATIONS CAPTURED FROM THE UPPER (X AXIS)

AND LOWER (Y AXIS) WABASH RIVERS. THE ρ VALUES OBTAINED FROM THIS AND

THE OTHER BIVARIATE COMBINATIONS (N = 21) WERE USED TO ASSESS THE

SPATIAL EXTENT TO WHICH SILVER CARP SYNCHRONOUSLY RECRUIT.