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Temporal Change in Crayfish Communities and links to a Changing Environment by Brie Anna Edwards A thesis submitted in conformity with the requirements for the degree of Doctor of Philosophy Department of Ecology and Evolutionary Biology University of Toronto © Copyright by Brie A. Edwards 2013
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  • Temporal Change in Crayfish Communities and links to a Changing Environment

    by

    Brie Anna Edwards

    A thesis submitted in conformity with the requirements for the degree of Doctor of Philosophy

    Department of Ecology and Evolutionary Biology University of Toronto

    © Copyright by Brie A. Edwards 2013

  • ii

    Temporal Change in Crayfish Communities and links to a

    Changing Environment

    Brie A. Edwards

    Doctor of Philosophy

    Department of Ecology and Evolution University of Toronto

    2013

    Abstract

    Community ecology and conservation are complementary disciplines under the umbrella of

    ecology, providing insight into the factors that determine where and how communities exist, and

    informing efforts aimed at sustaining the diversity and persistence of the organisms that comprise

    them. Conservation ecologists apply the principles of ecology and other disciplines, to the

    maintenance of biodiversity. This thesis uses this approach to assess the status of freshwater

    crayfish in south-central Ontario and investigate potential anthropogenic drivers of crayfish

    community change. I start with a temporal analysis of crayfish relative abundance over a period

    of 18 years and find that all species have experienced significant population declines across the

    sampled range, resulting in reduced species distributions and crayfish community diversity.

    Next I employ multivariate statistical techniques to relate changes in crayfish communities

    between the two time periods to ecological and anthropogenic changes. I identify a number of

    threats in the region that are correlated with crayfish decline and are likely to pose a threat to

    aquatic ecosystems more broadly in the region, including calcium (Ca) decline, metal pollution,

    human development, and species introductions. In the latter two chapters I look more closely at

    Ca decline as a mechanism driving crayfish declines. First, laboratory analysis of the effect of Ca

    availability on juvenile Orconectes virilis (a Shield native) reveals that survival is significantly

  • iii

    reduced below 0.5-0.9 mg·L-1, which is one of the lowest ever reported Ca requirement

    thresholds for a crustacean. Second, a correlative study using adult inter-moult crayfish collected

    from lakes that range broadly in their Ca concentrations, indicates that for O. virilis, carapace Ca

    content is significantly related to lake Ca concentration, and is under-saturating below 8 mg·L-1.

    This collective body of work identifies significant anthropogenic threats to crayfish and their

    aquatic ecosystems in south-central Ontario.

  • iv

    Acknowledgments Before anyone else, I have to thank Ron Reid, my first real science mentor and a lasting friend,

    for sharing his contagious love of benthic critters and crayfish, and encouraging me to become a

    researcher. Next, I thank my co-supervisors Don Jackson and Keith Somers, without whom none

    of this would have been possible. Keith saw potential in me that I didn’t know was there,

    introduced me to Don, and got the whole project off the ground. He has been a fantastic mentor,

    teacher, promoter and constructive critic, for which I am truly grateful. From Don I have learned

    more about the world, ecology, and myself than I have from any other influence in my life. He

    has mentored me with patience and generosity, and challenged me to exceed even my own

    expectations. I will be forever thankful for his support, within and beyond academia. I further

    thank my committee members Nick Collins and Harold Harvey for great discussions, sage

    advice, and unwavering positivity. This work wouldn’t have been possible without an excellent

    team of people to assist in the lab and field, so many thanks go out to Ellen Fanning, Amir

    Lewin, Vern Lewis, Simona Tencaliuc, Jesse Elders, and Kraig Picken.

    I consider myself extremely lucky to have had the opportunity to work with and be guided by

    Helen Rodd. She has encouraged and bolstered me through many highs and lows, has always

    been there to listen or to laugh, and has become a true friend and inspiration. I am also forever

    grateful for the lasting friendships and many things I have learned from and shared with lab

    mates and fellow candidates over the years, including Maggie Neff, Monica Granados, Meg

    Eizenman, Bronwyn Rayfield, Maria Bennell, Cam Weadick, Anna Price, Caren Scott, Steve

    Walker, Sapna Sharma, Mark Poesch, Andrew Drake, Angela Streker, Karen Alofs, Dak de

    Kerckhove, Aleks Polakowska, Jonathan Ruppert, Crystal Vincent, and Alex De Serrano.

    My extended families and dear friends outside academia are too numerous to name, but I owe

    each and every one of you endless thanks for supporting and encouraging me in your unique

    way. I would like to thank my parents Craig Edwards and Nepher Lewis for immersing me in

    the outdoors since birth and instilling in me an appreciation for the natural world that started me

    on the path toward a career in ecology. I thank my brother Colgan Edwards for sharing that

    enchanted path with me as we grew, and for being my best friend and biggest fan for as long as I

    can remember. Finally, I thank my incredible partner Kraig Picken, for helping me in every way

    imaginable throughout this journey. He sacrificed, collaborated, constructed, brainstormed, and

  • v

    problem solved right along with me, and even proved himself a superior crayfish diver, as hard

    as it is to admit. His fierce adoration and pride in my work was a driving force from the start to

    the finish of this degree and over every bump along the way. Special mention goes out to my

    son, Fisher Picken, whose arrival revived my curious mind and gave me the renewed perspective

    and balance that carried me through the final year.

  • vi

    Table of Contents Acknowledgments.......................................................................................................................... iv

    Table of Contents........................................................................................................................... vi

    List of Tables .................................................................................................................................. x

    List of Figures ................................................................................................................................ xi

    List of Appendices ....................................................................................................................... xiv

    Chapter 1 General Introduction ...................................................................................................... 1

    References....................................................................................................................................... 8

    Chapter 2 Multispecies crayfish declines in lakes: implications for species distributions and richness..................................................................................................................................... 14

    2.1 Abstract ............................................................................................................................. 14

    2.2 Introduction....................................................................................................................... 14

    2.2.1 Study Lakes and Study Region ............................................................................. 16

    2.3 Methods............................................................................................................................. 18

    2.3.1 Site selection and crayfish sampling..................................................................... 18

    2.3.2 Chemistry sampling .............................................................................................. 19

    2.3.3 Data analysis ......................................................................................................... 19

    2.4 Results............................................................................................................................... 21

    2.4.1 Crayfish................................................................................................................. 21

    2.4.2 Water chemistry .................................................................................................... 26

    2.5 Discussion ......................................................................................................................... 29

    2.5.1 Crayfish trends ...................................................................................................... 29

    2.5.2 Potential environmental links ............................................................................... 31

    2.5.3 General implications ............................................................................................. 34

    2.6 Acknowledgements........................................................................................................... 34

    References..................................................................................................................................... 35

  • vii

    Supplementary Tables and Figures............................................................................................... 40

    Copyright Acknowledgements...................................................................................................... 41

    Chapter 3 Temporal changes in crayfish communities and environmental change...................... 42

    3.1 Abstract ............................................................................................................................. 42

    3.2 Introduction....................................................................................................................... 42

    3.3 Materials and Methods...................................................................................................... 44

    3.3.1 Crayfish assemblage data...................................................................................... 44

    3.3.2 Environmental matrices ........................................................................................ 44

    3.3.3 Statistical Analyses ............................................................................................... 47

    3.4 Results............................................................................................................................... 50

    3.5 Discussion ......................................................................................................................... 55

    3.5.1 Assemblage patterns ............................................................................................. 55

    3.5.2 Ecological Drivers ................................................................................................ 57

    3.5.3 Implications for Lake Ecosystems ........................................................................ 59

    3.6 Acknowledgements........................................................................................................... 61

    References..................................................................................................................................... 62

    Supplementary Tables and Figures............................................................................................... 67

    Copyright Acknowledgements...................................................................................................... 71

    Chapter 4 Effects of calcium (Ca) availability on the survival, growth, and Ca content of freshwater crayfish, Orconectes virilis, originating from waters experiencing [Ca] decline .. 72

    4.1 Abstract ............................................................................................................................. 72

    4.2 Introduction....................................................................................................................... 72

    4.3 Methods............................................................................................................................. 74

    4.3.1 Crayfish................................................................................................................. 74

    4.3.2 Experimental Design............................................................................................. 75

    4.3.3 Statistical Analyses ............................................................................................... 76

  • viii

    4.4 Results............................................................................................................................... 77

    4.4.1 Survival ................................................................................................................. 77

    4.4.2 Ca Content ............................................................................................................ 78

    4.4.3 Growth and Moulting............................................................................................ 79

    4.5 Discussion ......................................................................................................................... 81

    4.6 Acknowledgements........................................................................................................... 84

    References..................................................................................................................................... 85

    Chapter 5 Evaluating the effect of lake calcium concentration on the acquisition of carapace calcium by freshwater crayfish ................................................................................................ 88

    5.1 Abstract ............................................................................................................................. 88

    5.2 Introduction....................................................................................................................... 88

    5.3 Methods............................................................................................................................. 90

    5.3.1 Crayfish Collection ............................................................................................... 90

    5.3.2 Analytical Techniques .......................................................................................... 92

    5.3.3 Statistical Analyses ............................................................................................... 93

    5.4 Results............................................................................................................................... 93

    5.5 Discussion ......................................................................................................................... 97

    5.6 Acknowledgements......................................................................................................... 100

    References................................................................................................................................... 101

    Chapter 6 General Conclusion .................................................................................................... 103

    References................................................................................................................................... 107

    Appendix 1. Lake Information.................................................................................................... 110

    Appendix 2. Historical Lake Chemistry ..................................................................................... 114

    Appendix 3. Current Lake Chemistry......................................................................................... 116

    Appendix 4. Presence/Absence of Predatory Fish...................................................................... 118

    Appendix 5. Historical Crayfish Survey Data ............................................................................ 120

  • ix

    Appendix 6. Current Crayfish Survey Data................................................................................ 124

    Appendix 7. 2009 Juvenile Experiment Data ............................................................................. 127

    Appendix 8. 2010 Juvenile Experiment Data ............................................................................. 129

    Appendix 9. Carapace Broad Survey Sample Data .................................................................... 131

    Appendix 10. Red Chalk East Carapace Sample Data ............................................................... 135

  • x

    List of Tables Table 2-1. Results of the model II regression analyses comparing current and historical relative

    abundances (Catch Per Unit Effort [CPUE]) for all lakes in which a species was found. n = the

    number of lakes in which a species was found, p = probability associated with the difference

    from the null expectation (1:1), % historical = the percentage of lakes in which the species

    occurred historically that have current populations of the species. .............................................. 20

    Table 2-2. Chemical variables that changed significantly in all study lakes or in the Shield lakes

    between the historical survey and the current study. Δ = % change, Alkti = alkalinity, DIC =

    dissolve inorganic C, p = probability associated with paired t-tests comparing current and

    historical values, * indicates differences were significant only in Shield lakes and means and Δ

    apply only to Shield lakes, ns = not significant (p > 0.05). .......................................................... 26

    Table 3-1. Summary information for all environmental variables in the crayfish-containing lakes

    (66 historical and 57 current) considered in the analyses. ............................................................ 46

    Table 3-2. Pearson correlations and significance for indirect analyses of the association of

    environmental variables with the principal component axes from the ordinations of community

    data (Fig. 2) as well as unique community variation constrained by each environmental variable

    in the RDA ordinations (Fig. 3). ................................................................................................... 49

    Table 4-1. Percentage of replicate individuals in each treatment in both years that were observed

    to moult ≥ 1 or ≥ 2 times over the course of the experiment, and the mean ± SE moult increment

    (in days) from individuals who moulted two or more times......................................................... 80

    Table 5-1. General characteristics of each lake sampled (south-central Ontario) and

    corresponding crayfish specimen information, ordered by lake [Ca]........................................... 91

    Table 5-2. Variables considered in the step-wise multiple regression model predicting individual

    O. virilis carapace Ca content (%) using (a) the full multi-lake survey samples and (b) the Red

    Chalk East population sample, with the percentage of the explained variation in carapace Ca

    content associated with each variable in the final model.............................................................. 97

  • xi

    List of Figures Figure 2-1. Study region in Ontario, Canada, showing the 100 lakes surveyed. Tertiary

    watersheds are delineated and identified by the following codes: 2EA = Georgian Bay tributaries,

    2EB = Moon and Go Home rivers, 2EC = Severn River, 2HF = Cameron Lake drainage, 2CF =

    Sudbury Region, 2KD = Upper Madawaska River, 2KB = Deep River, 2HH = Kawartha Lakes

    region, 2HG = Scugog River. ....................................................................................................... 17

    Figure 2-2. Model II regression plots for current vs historical abundance (as catch per unit effort

    [CPUE]) of Orconectes virilis (A), O. propinquus (B), O. immunis (C), O. obscurus (D),

    Cambarus bartonii (E), and C. robustus (F), in relation to the 1:1 null expectation (dashed line).

    Insets show details for species with many low abundances. ........................................................ 22

    Figure 2-3. Frequency distributions of crayfish species richness in the historical and current

    surveys. ......................................................................................................................................... 23

    Figure 2-4. Changes in the number of lakes with populations of Orconectes virilis (O.v.), O.

    propinquus (O.p.), O. immunis (O.i.), O. obscurus (O.o.), O. rusticus (O.r.), Cambarus bartonii

    (C.b.), and C. robustus (C.r.), between the historical and current surveys in relation to the 1:1

    null expectation (dashed line). ...................................................................................................... 24

    Figure 2-5. Distributions of Orconectes propinquus (A), O. virilis (B), Cambarus bartonii (C),

    and C. robustus (D), indicating populations that appear stable, have declined by ≥50%, appear to

    have been lost, or were newly detected. ....................................................................................... 25

    Figure 2-6. Model II regression plots for log(x) transformed current vs historical alkalinity

    (Alkti) (A), Al (B), Ca* (C), Cl (D), dissolved organic C (DIC*) (E), Mg* (F), Na (G), NO3 (H),

    and SO4 (I), in relation to the 1:1 null expectation (dashed line). Off-Shield lakes are designated

    by open circles. A constant of 1 (2 in the case of alkalinity) was added before transformation of

    Al, Cl, DIC, Mg, Na, and NO3. * indicates differences were significant only in Shield lakes and

    so off-Shield lakes were excluded from analysis.......................................................................... 28

    Figure 3-1. Map of south-central Ontario indicating the survey range in dark shading, with an

    inset of the location in the broader Great Lakes region. ............................................................... 45

  • xii

    Figure 3-2. Flow diagram to illustrate the organization of data matrices and which matrices were

    involved in the various ordination techniques employed to answer the basic research questions.

    The ‘H’ and grey fill indicate historical data, and the C and white fill indicate current data....... 48

    Figure 3-3. Principal component analysis ordination of community data from the historical (a)

    and current (b) surveys. Lakes are identified by a two letter code (see Appendix 1)................... 51

    Figure 3-4. Redundancy analysis ordination of community data constrained by environmental

    predictors from the historical (a) and current (b) surveys............................................................. 53

    Figure 3-5. Redundancy analysis ordination of community data from the combined historical and

    current surveys constrained by environmental predictors including time period. Historical sites

    are white and current sites are grey............................................................................................... 55

    Figure 4-1. Percent of replicate individuals in each treatment surviving on each day over the 12

    week experiment in 2009. ............................................................................................................. 78

    Figure 4-2. Percent of replicate individuals in each treatment surviving on each day over the 12

    week experiment in 2010. ............................................................................................................. 78

    Figure 4-3. Box plots indicating the median (heavy line) and distribution of calcium contents (%)

    of replicate individuals in each treatment in both years. Box edges indicate the first and third

    quartiles, and whiskers represent the nearest value within [quartile values ± 1.5 x Inter Quartile

    Range]. Outliers are represented by open circles.......................................................................... 79

    Figure 4-4. Box plots indicating the median (heavy line) and distribution of growth rates (mg

    day-1) of replicate individuals in each treatment in both years. Box edges indicate the first and

    third quartiles, and whiskers represent the nearest value within [quartile values ± 1.5 x Inter

    Quartile Range]. Outliers are represented by open circles. .......................................................... 80

    Figure 5-1. Carapace of an O. rusticus specimen after removal (a), followed by rinsing with

    deionized water and obtaining a hole punch from the posterior region (b). ................................. 92

    Figure 5-2. Relationships between carapace Ca content (mean % ± SE) and lake [Ca] (mg·L-1)

    for O. virilis (black fill), O. rusticus (white fill), and C. bartonii (grey fill). Points represent mean

    ±SE for each sampled population, and simple linear regression lines are indicated for O. virilis

  • xiii

    (solid) and O. rusticus (dashed). Inset provides an expanded view of the cluster of lakes with

    [Ca] < 4 mg·L-1. ............................................................................................................................ 94

    Figure 5-3. Relationships between carapace Ca content (mean % ± SE) and lake [Ca] (mg·L-1)

    for O. virilis (black fill), O. rusticus (white fill) in their shared range of [Ca] > 8 mg·L-1. Points

    represent mean ± SE for each sampled population, and simple linear regression lines are

    indicated for O. virilis (solid) and O. rusticus (dashed). .............................................................. 95

    Figure 5-4. Logarithmic relationship (solid black line) between carapace Ca content (mean % ±

    SE) and lake [Ca] (mg·L-1) for collected O. virilis (filled circles) across the broad survey range,

    indicating that conditions may be sub-saturating below 8 mg·L-1. The three reference lake

    samples from France (1987) have been added to the plot (open squares) for comparative

    purposes. ....................................................................................................................................... 96

    Figure 5-5. Relationships between carapace Ca content (%) and categories of carapace hardness

    (HS: hard-soft, H: hard, VH: very hard) for O. virilis. Bars represent mean ± SE of individuals

    for each category........................................................................................................................... 96

    Figure 5-6. Relationships between carapace Ca content (%) and (a) carapace length (mm) and (b)

    carapace hardness category (SH: soft-hard, HS: hard-soft, H: hard, VH: very hard) in the O.

    virilis individuals sampled from Red Chalk East Lake. Panel (a) differentiates male individuals

    (open circles) from female individuals (filled circles). Bars on panel (b) represent mean ± SE of

    individuals for each category. ....................................................................................................... 97

  • xiv

    List of Appendices Appendix 1. Lake Information.................................................................................................... 110

    Appendix 2. Historical Lake Chemistry ..................................................................................... 114

    Appendix 3. Current Lake Chemistry......................................................................................... 116

    Appendix 4. Presence/Absence of Predatory Fish...................................................................... 118

    Appendix 5. Historical Crayfish Survey Data ............................................................................ 120

    Appendix 6. Current Crayfish Survey Data................................................................................ 124

    Appendix 7. 2009 Juvenile Experiment Data ............................................................................. 127

    Appendix 8. 2010 Juvenile Experiment Data ............................................................................. 129

    Appendix 9. Carapace Broad Survey Sample Data .................................................................... 131

    Appendix 10. Red Chalk East Carapace Sample Data ............................................................... 135

  • Chapter 1 General Introduction

    Two important sub-disciplines under the umbrella of ecology are community ecology and

    conservation. In many ways, these two sub-disciplines are complements to one another,

    providing insight into the factors that determine where and how communities exist, as well as

    informing efforts aimed at sustaining the diversity and persistence of the organisms that

    comprise them (Smith and Smith 2006). A fundamental goal in community ecology is to

    understand the environmental constraints on species distributions and the factors affecting

    assemblage patterns, and the primary applications of this field of study are related to global

    change and conservation (Simberloff 2004, Smith and Smith 2006). Fueled by a growing

    appreciation for the impacts of anthropogenic activities on natural ecosystems, conservation

    ecologists apply the principles of population and community ecology, as well as many additional

    disciplines to the maintenance of biodiversity (Smith and Smith 2006). One of the most pressing

    issues in the field today is bridging the gap between conservation assessment and the

    implementation of conservation action (Knight et al. 2008, Lysne et al. 2008). Despite a number

    of notable instances where good models of populations and communities have enabled successful

    predictions and management actions in relation to conservation and invasive species,

    improvements in our ability to detect and quantify threats, their interactions, and predicted

    outcomes are necessary in order to inform effective conservation measures (Simberloff 2004,

    Venter et al. 2006, Rands et al. 2010, Amano 2012).

    Freshwater ecosystems are more threatened than any other system on the planet (Master 1991,

    Jelks et al. 2008, Magurran 2009, Abell et al. 2011) and freshwater species are disappearing at a

    rate five times that of terrestrial animals (Ricciardi & Rasmussen 1999). Despite this situation,

    freshwater conservation has continually lagged behind that of terrestrial and marine systems

    (Amis et al. 2009). Aquatic communities, such as fish or benthic invertebrates, are thought to be

    structured by biotic and abiotic factors that operate on multiple temporal and spatial scales (Tonn

    1990, Smith and Powell 1971, Jackson et al. 2001, Mykra et al. 2007). Given the imperiled state

    of aquatic biota, it is important to understand how these factors structure communities, as well as

    how community membership can change over time and under anthropogenic influence. Aquatic

    systems face an ever-growing list of both local and regional anthropogenic impacts, including

    1

  • climatic warming, physical alteration and disturbance, various forms of chemical pollution,

    introductions of non-native species, and overexploitation for human uses (Allan and Flecker

    1993, Wilcove et al. 1998), which have collectively led to widespread habitat loss, water quality

    degradation, reductions in ecosystem function and stability, and the loss of biodiversity

    (Williams et al. 1989, Revenga et al. 2000, Jelks et al. 2008, Magurran 2009). There is a growing

    body of literature documenting the extent to which aquatic species have been negatively affected

    by environmental changes in North America (e.g. Williams et al. 1989, Stuart et al. 2004, Taylor

    et al. 2007, Jelks et al. 2008). However, beyond some well studied fish populations, researchers

    in general have yet to quantitatively relate declines in particular community members to specific

    environmental or anthropogenic influences.

    Communities that are sensitive to biotic and abiotic characteristics of environmental change and

    that influence ecosystem structure or function are important for identifying the most influential

    stressors on aquatic ecosystems. Crayfish are a good choice by these criteria because their

    relative abundance is driven by the specific chemical and physical conditions of their aquatic

    environments (Capelli and Magnusson 1983, France and Collins 1993, Larson and Olden 2013).

    Crayfish have historically been used as biological indicators of environmental condition in

    relation to anthropogenic stressors such as contamination by heavy metals (Alikhan et al. 1990)

    and lake acidification (Reid and David 1990, Somers et al. 1996, David et al. 1997). Crayfish

    also greatly influence the structure and function of the ecosystems they inhabit by physically

    modifying aquatic habitats and altering the flow of energy through the food chain (Momot 1995,

    Creed and Reed 2004).

    Despite their importance in aquatic ecosystems and potential for use as biological indicators,

    North American crayfish have received less conservation attention than other freshwater taxa

    (Taylor et al. 1996, 2007). Information on the status of crayfish in Canada is even more limited

    (Hamr 1998, 2006, Guiasu 2007), however several native populations in lakes in south-central

    Ontario were shown to have experienced significant declines (David et al. 1994), potentially

    indicating broader ecological issues in the region. Ontario is the crayfish biodiversity hotspot in

    Canada, and is home to 9 of the 11 species that can be found nationwide, including natives

    Fallicambarus fodiens, Cambarus diogenes, C. bartonii, C. robustus, Orconectes immunis, O.

    propinquus, and O. virilis, as well as non-natives O. obscurus and O. rusticus. There is evidence

    that effective conservation initiatives should focus on biodiversity hotspots, where efforts are

    2

  • likely to have a greater overall impact (Dobson et al. 1997, Myers et al. 2000). Conservation

    assessment and then local (state, provincial) or national protection is needed where endangered

    or threatened species of crayfish are identified (Taylor et al. 2007, Crandal and Buhay 2008).

    The longer a species is recognized as threatened or at risk, the greater its chances of recovery

    (Taylor et al. 2005). Therefore, the driving objective of this thesis was to ascertain the status of

    crayfish in south-central Ontario lakes, and to identify any contributing environmental threats.

    Very little is known about the environmental factors that shape the membership and relative

    abundances of crayfish communities. However, research has shown that the occurrence and

    relative abundance of crayfish in lakes may be related to a wide variety of factors including pH

    (France and Collins 1983, Davies 1989, France 1993, Seiler and Turner 2004), water temperature

    (Somers and Green 1993, Jiravanichpaisal et al. 2004, Hammond et al. 2006), calcium (Ca)

    availability (France 1987, Keller et al. 2001, Rukke 2002, Hammond et al. 2006), lake

    morphology (Jones and Momot 1981), productivity (Jones and Momot 1981, France 1985),

    predators (Collins et al. 1983, Hill and Lodge 1995, Nystrom et al. 2006), other crayfish species

    (Hill and Lodge 1999), and anthropogenic habitat alteration (Schultz et al. 2006).

    The inland lakes of central Ontario, once considered pristine, increasingly face the full spectrum

    of top-ranked anthropogenic impacts to aquatic ecosystems world wide (Allan and Flecker 1993,

    Wilcove et al. 1998, Venter et al. 2006), including: the introduction of new fish predators such as

    smallmouth bass; new crayfish competitors such as the rusty crayfish; habitat degradation related

    to shore development; pollution and chemical change related to acidification and metal

    contamination; and the depletion of cations such as Ca.

    Physical habitat alteration and increased recreational development of some lakes in the region

    has been noted (e.g., Molot and Dillon 2008, Yan et al. 2008) but not directly quantified.

    Crayfish preferentially inhabit the near-shore littoral zone of lakes (Jones and Momot 1981).

    Depending on the species, crayfish use rocks, macrophyte beds, and coarse woody debris as

    refugia (Nystrom et al. 2006) and, in some cases, construct depressions and burrows as long- or

    short-term dwellings (Crocker and Barr 1968). As the number of cottages and recreational homes

    around the lakes increase, natural shorelines are transformed, and undesired (by homeowners)

    substrates, plants, and materials are removed (Christensen et al. 1996) and often are replaced

    with sand. Such alterations result in less suitable habitat for crayfish and could lead to crowding

    3

  • and increased competition, cannibalism, and predation. Nutrient inputs also increase with the

    number of dwellings present in a watershed, often with eutrophying effects (Carpenter et al.

    1998, Moore et al. 2003). Species range in their tolerance to trophic conditions in lakes, but all of

    Ontario’s open-water crayfish, except O. immunis, are thought to prefer, cool, clear, well-

    oxygenated conditions (Crocker and Barr 1968, Capelli 1975, Berrill 1978).

    Introductions of smallmouth bass (Micropterus dolomieui) have occurred across the study

    region, and the range of smallmouth bass is predicted to expand because of continued illegal

    angler introductions and climate change (MacRae and Jackson 2001,Vander Zanden et al. 2004,

    Sharma and Jackson 2008). Smallmouth bass are voracious predators of crayfish (Crocker and

    Barr 1968, Collins et al. 1983, Somers and Green 1993, Taylor et al. 2005). Crayfish abundance

    (as CPUE) often decreases in the presence of smallmouth bass because of predation-induced

    mortality or reduced catchability caused by predator-avoidance behavior (Collins et al. 1983, Hill

    and Lodge 1995, Nystrom et al. 2006).

    At the outset of this study, it was unclear whether the presence of nonnative crayfish was

    potentially negatively impacting native species. Orconectes rusticus is thought to have very

    similar environmental preferences to, and competitive dominance over O. virilis and O.

    propinquus, frequently leading to their replacement (Lodge et al. 1986, Olden et al. 2006, Olden

    et al. 2011). Abundances of native crayfish species might have declined when lakes were first

    invaded by the two nonnative crayfish species, O. rusticus and O. obscurus, particularly in lakes

    south of the Shield where O. rusticus was introduced (Berrill 1978, David et al. 1997, Wilson et

    al. 2004). However, crayfish can no longer legally be sold as bait or be transported between

    water bodies in Ontario because of concern that O. rusticus could invade new habitats.

    Moreover, water-chemistry issues, such as low Ca concentrations, might prevent the

    establishment of O. rusticus in the hundreds of thousands of lakes on the Canadian Shield

    (Edwards et al. 2013). However, the realized current ranges of these two species were unknown

    previous to this dissertation research.

    One particularly promising hypothesis regarding drivers of crayfish declines in the region relates

    to historical acidification and metal contamination caused by the long-range transport of

    sulphuric and nitric acid precursors, which have significantly altered water chemistry throughout

    the inland Canadian Precabrian Shield (hereafter referred to as ‘Shield’) lakes of south-central

    4

  • Ontario (Stoddard et al. 1999, Keller et al 2003). A side effect of the subsequent acidification

    recovery in lakes and reduced cation leaching from the surrounding soils has been the reduction

    of major cations, including Ca (Whatmough and Dillon 2003, Jeziorski et al. 2008, Molot and

    Dillon 2008, Watmough and Aherne 2008). Calcium concentrations in watershed soil pools and

    surface waters are now well below pre-acidification levels (Stoddard et al. 1999, Watmough and

    Dillon 2003, Jeziorski et al. 2008), and lake concentrations are predicted to continue to drop 10

    to 40% from their current levels (Watmough and Aherne 2008).

    Calcium is an essential element for most biota. In addition to many physiological roles, crayfish

    must acquire Ca for the formation of exoskeletons and might experience increased metabolic

    costs in low-Ca environments (Greenaway 1974, Cairns and Yan 2009). Changes in Ca

    acquisition could make crayfish more vulnerable to predation, cannibalism, or competition, and

    impact their growth, survival, and reproductive success (Stein 1977, France 1987, Keller et al.

    2001, Rukke 2002, Hammond et al. 2006, Cairns and Yan 2009). Calcium concentrations in

    many of south-central Ontario’s Shield lakes are now

  • Research Overview

    My first two thesis chapters investigate the status and ecology of freshwater crayfish in south-

    central Ontario in the context of temporal change. In Chapter 2 I quantify temporal change in

    crayfish populations from 100 lakes in south-central Ontario using two sampling periods

    separated by approximately 20 years. I further assess the spatial and taxonomic breadth of these

    changes, and relate trends to quantified environmental changes over the same period. I found

    that the majority of populations of all species detected in the study region have declined severely

    between sampling periods, and that widespread population losses have resulted in reduced

    crayfish community diversity and shrunken or patchy species distributions. Several significant

    environmental changes were identified in the region, which may be implicated as contributing to

    the declines observed in crayfish. These include physiochemical changes, such as calcium

    decline, inputs of aluminum, chloride and nutrients, shore development, and near-shore warming,

    as well as the introduction of centrarchid predatory fish.

    In Chapter 3 I use multivariate ordination techniques to identify important environmental drivers

    of crayfish relative abundance and community composition, both historically and currently using

    the south-central Ontario survey data. I further identify changes in species-environment

    relationships and temporal changes in crayfish assemblages between the historical and current

    surveys, in order to elucidate emerging threats to aquatic systems in the region. I found that

    community composition had changed significantly between the two time periods, and that the

    importance of anthropogenic stressors in driving crayfish abundance had increased relative to

    natural drivers. In particular, my results indicate that nutrient inputs and shore development from

    increasing human activities, the invasion of warm-water centrarchid fishes, and chemical

    changes such as acidification and calcium decline, as well as increases in aluminum, appear to be

    driving crayfish declines.

    My last two thesis chapters focus on the relationship between environmental calcium availability

    and various aspects of freshwater crayfish biology, in order to assess the potential for regional Ca

    declines to negatively impact crayfish populations in south-central Ontario.

    6

  • In Chapter 4 I conduct laboratory experiments to determine the effects of [Ca] on the growth, Ca

    acquisition, and survival of juvenile O. virilis originating from a region experiencing Ca decline.

    I found that neither growth nor whole-body calcium content was affected by Ca availability.

    Survivorship, however, was significantly reduced at 0.5 – 0.9 mgL-1. This acute tolerance

    threshold is lower than any other studied freshwater crayfish species, and might indicate that the

    species will be able to persist under forecast [Ca] of lakes in regions experiencing [Ca] decline.

    However, the additional pressures imposed in a natural setting will likely increase this

    requirement above our lab based determination, making actual outcomes difficult to predict.

    In Chapter 5 I use field collections of O. virilis, O. rusticus, and C. bartonii from lakes over a

    broad range of [Ca], in order to describe the relationship between the availability of aquatic Ca

    and the incorporation of Ca into adult carapaces at intermolt. I find that carapace Ca content is

    significantly positively related to lake [Ca] in O. virilis, and that lake [Ca] appears to become

    saturating for this species at approximately 8 mgL-1. The results further indicate that the

    carapace Ca content of O. virilis is also significantly positively related to carapace hardness

    (rigidity) and the size of the individual, but is not significantly related to sex. No significant

    relationship was detected between carapace Ca and lake [Ca] in either C. bartonii or O. rusticus,

    most likely because they were sampled over a comparatively small range of lake [Ca]. Overall

    this study indicates that despite some individual level variability, O. virilis is experiencing low

    [Ca] stress in the majority of soft-water Boreal Shield lakes undergoing Ca declines throughout

    its range.

    Chapters 2 and 3 are published or in press, and have been included in this thesis with permission

    from the publishers:

    Edwards, B.A., Jackson, D.A., and Somers, K.M. 2009. Multispecies crayfish declines in lakes:

    implications for species distributions and richness. Journal of the North American Benthological

    Society 28: 719-732.

    Edwards, B.A., Jackson, D.A., and Somers, K.M. In Press. Linking temporal changes in crayfish

    communities to environmental changes in boreal Shield lakes in south-central Ontario. Canadian

    Journal of Fisheries and Aquatic Sciences.

    7

  • References Abell, R., Thieme, M., Ricketts, T. H., Olwero, N., Ng, R., Petry, P., Dinerstein, E., Revenga, C.,

    and Hoekstra, J. 2011. Concordance of freshwater and terrestrial biodiversity. Conservat. Lett. 4: 127-136.

    Alikhan, M.A., Bagatto, G., and Zia, S. 1990. The crayfish as a “biological indicator” of aquatic contamination by heavy metals. Wat. Res. 24: 1069-1076.

    Allan, J.D., and Flecker, A.S.1993. Biodiversity conservation in running waters. BioSci. 43(1): 32-43.

    Amano, T. 2012. Unraveling the dynamics of organisms in a changing world using ecological modeling. Ecol. Res. 27: 495-507.

    Amis, M. A., Rouget, M., Lotter, M., and Day, J.2009. Integrating freshwater and terrestrial priorities in conservation planning. Biological Conservation 142: 2217-2226.

    Berrill, M. 1978. Distribution and ecology of crayfish in the Kawartha region of southern Ontario. Can. J. Zool. 56: 166-177.

    Cairns, A, and Yan, N. 2009. A review of the influence of low ambient calcium concentrations on fresh water daphnids, gammarids and crayfish. Envoron. Rev. 17: 67-79.

    Capelli, G.M. 1975. Distribution, life history, and ecology of crayfish in northern Wisconsin, with emphasis on Orconectes propinquus (Girard). Ph.D. Thesis, University of Wisconsin, Madison. Pp 1-214.

    Capelli, G.M, and Magnusson, J.J. 1983. Morphoedaphic and biogeographic analysis of crayfish distribution in Northern Wisconsin. J. Crust. Biol. 3(4): 548-564.

    Carpenter, S.R., Caraco, N.F., Correll, D.L., Howarth, R.W., Sharpley, A.N., and Smigh, V.H. 1998. Nonpoint pollution of surface waters with phosphorus and nitrogen. Ecol. App. 8: 559-568.

    Carpenter, S.R. Benson, B.J., Biggs, R., Chipman, J.W., Foley, J.A., Golding, S.A., Hammer, R.B., Hanson, P.C., Johnson, P.T.J., Kamarainen, A.M., Kratz, T.K., Lathrop, R.C., McMahon, K.D., Provencher, B., Rusak, J.A., Solomon, C.T., Stanley, E.H., Turner, M.G., Vander Zanden, M.J., Wu, C.-H., and Yuan, H. 2007. Understanding regional change: a comparison of two lake districts. BioSci. 57: 323-335.

    Christensen, D.L., Herwig, B.R., Schindler, D.E., and Carpenter, S.R. 1996. Impacts of lakeshore residential development on coarse woody debris in north temperate lakes. Ecol. App. 6:1143-1149.

    Collins, N.C., Harvey, H.H., Tierney, A.J., and Dunham, D.W. 1983. Influence of predatory fish density on trapability of crayfish in Ontario Lakes. Can. J. Fish. Aquat. Sci. 40: 1820-1828.

    Crandal, K.A., and Buhay, J.E. 2008. Global diversity of crayfish (Astacidae, Cambaridae, and Parastacidae—Decapoda) in freshwater. Hydrobiologia 595: 295–301.

    Creed, R.P., Jr., and Reed, J.M. 2004. Ecosystem engineering by crayfish in a headwater stream community. J. N. Am. Benthol. Soc. 23(2): 224-236.

    8

  • Crocker, D.W., and Barr, D.W. 1968. Handbook of the crayfishes of Ontario. University of Toronto Press, for the Ontario Ministry of the Environment, Toronto, Ontario.

    Davies, I.J. 1989. Population collapse of the crayfish Orconectes virilis in response to experimental whole-lake acidification. Can. J. Fish. Aquat. Sci. 46: 910-922

    David, S.M., Somers, K.M., and Reid, R.A.. 1994. Long-term trends in the relative abundance of crayfish from acid sensitive, softwater lakes in south central Ontario: a data summary for the first 5 years, 1988 – 1992. Ontario Ministry of the Environment, Dorset, ON, ISBN 0-7778-1924-4, 38 pp. + app.

    David, S.M., Somers, K.M., Reid, R.A., and Ingram, R.I. 1997. Crayfish species assemblages in softwater lakes in seven tertiary watersheds in south-central Ontario. Ontario Ministry of the Environment, Dorset, ON, ISBN 0-7778-6504-1, 102 pp.

    Edwards, B.A., Lewis, V.R.E., Rodd, F.H., and Jackson, D.A. 2013. Interactive effects of calcium decline and predation risk on the potential for a continuing northward range expansion of the rusty crayfish (Orconectes rusticus). Can. J. Zool. 91: 328-337.

    Dobson, A.P., Rodriquez, J.P., Roberts, W.M., and Wilcove, D.S. 1997. Geographic distribution of endangered species in the United States. Science 275: 550-553.

    France, R.L. 1985. Relationship of crayfish (Orconectes virilis) growth to population abundance and system productivity in small oligotrophic lakes in the Experimental Lake Area, northwestern Ontario. Can. J. Fish. Aquat. Sci. 42: 1096-1102.

    France, R.L. 1987. Calcium and trace metal composition of crayfish (Orconectes virilis) in relation to experimental lake acidification. Can. J. Fish. Aquat. Sci. 44 (Suppl. 1): 107-113.

    France, R.L. 1993. Influence of lake pH on the distribution, abundance and health of crayfish in Canadian Shield lakes. Hydrobiologia 271: 65-70.

    France, R.L., and Collins, N.C. 1993. Extirpation of crayfish in a lake affected by long-range anthropogenic acidification. Conservat. Biol. 7: 184-188

    Greenaway, P. 1974. Total body calcium and haemolymph calcium concentration sin the crayfish Austropotamobius pallipes (Lereboullet). J. Exp. Biol. 61: 19-26.

    Guiasu, R.C. 2007. Conservation and diversity of the crayfishes of the genus Fallicambarus Hobbs, 1969 (Decapoda, Cambaridae), with an emphasis on the status of Fallicambarus fodiens (Cottle, 1863) in Canada. Crustaceana 80(2): 207-223.

    Hammond, K.S., Hollows, J.W., Townsend, C.R., and Lokman, P.M. 2006. Effects of temperature and water calcium concentration on growth, survival and moulting of freshwater crayfish, Paranephrops zealandicus. Aquaculture 251: 271-9

    Hamr, P. 1998. Conservation status of Canadian freshwater crayfishes. World Wildlife Fund Canada, Toronto, Ontario.

    Hamr, P. 2006. The distribution and conservation status of burrowing crayfishes Fallicambarus fodiens and Cambarus diogenes in Canada. Freshwater Crayfish 15: 271-282.

    Hill, A.M., and Lodge, D.M. 1995. Multi-trophic-level impact of sublethal interactions between bass and omnivorous crayfish. J. N. Am. Benthol. Soc. 14(2): 306-14.

    9

  • Hill, A.M., and Lodge, D.M. 1999. Replacement of resident crayfishes by an exotic crayfish: the roles of competition and predation. Ecol. App. 9(2): 678-90.

    Jackson, D.A., Peres-Neto, P.R., and Olden, J.D. 2001. What controls who is where in freshwater fish communities – the roles of biotic, abiotic, and spatial factors. Can. J. Fish. Aquat. Sci. 58: 157-170.

    Jelks, H.L., Walsh, S.J., Burkhead, N.M., Contreras-Balderas, S., Diaz-Pardo, E., Hendrickson, D.A., Lyons, J., Mandrak, N.E., McCormick, F., Nelson, J.S., Platania, S.P., Porter, B.A., Renaud, C.B., Schmitter-Soto, J.J., Taylor, E.B., and Warren, M.L., Jr. 2008. Conservation status of imperiled North American Freshwater and Diadromous Fishes. Fisheries 33: 372-407.

    Jeziorski, A., Yan, N.D., Patterson, A.M., DeSellas, A.M., Turner, M.A., Jeffries, D.S., Keller, B., Weeber, R.C., McNicol, D.K., Palmer, M.E., McIver, K., Arseneau, K., Ginn, B.K., Cumming, B.F., and Smol, J.P. 2008. The widespread threat of calcium decline in fresh waters. Science 322: 1374–1377.

    Jiravanichpaisal, P., Soderhall, K., and Soderhall, I. 2004. Effect of water temperature on the immune response and infectivity pattern of white spot syndrome virus (WSSV) in freshwater crayfish. Fish. Shellfish. Immun. 17: 265-75.

    Jones, P.D., and Momot, W.T. 1981. Crayfish productivity, allochthony and basin morphology. Can. J. Fish. Aquat. Sci. 38(2): 175-183.

    Keller, W., Dixit, S.S., and Heneberry, J. 2001. Calcium declines in northeastern Ontario lakes. Can. J. Fish. Aquat. Sci. 58: 2011-20.

    Keller, W., Heneberry, J.H., and Dixit, S.S. 2003. Decreased acid deposition and the chemical recovery of Killarney, Ontario, lakes. Ambio 32: 183–189.

    Knight, A.T., Cowling, R.M., Rouget, M. Balmford, A., Lombard, A.T., and Campbell, B.M. 2008. Knowing but not doing: selecting priority conservation areas and the research-implementation gap. Conservat. Biol. 22: 610-617.

    Kozlova, T., Wood, C.M., and McGeer, J.C. 2009.The effect of water chemistry on the acute toxicity of nickel to the cladoceran Daphnia pulex and the development of a biotic ligand model. Aquat. Tox. 91: 221-228.

    Larson, E.R., and Olden, J.D. 2013. Crayfish occupancy and abundance in lakes of the Pacific Northwest, USA. Freshw. Sci. 32: 94-107.

    Lindberg, T.T., Bernhardt, E.S., Bier, R., Helton, A.M., Merola, R.B., Vengosh, A., and Di Giulio, D.T. 2011. Cumulative impacts of mountaintop mining on an Appalachian watershed. Proceed. Nat. Acad. Sci. 108: 20929-20934.

    Lodge, D.M., Kratz, T.K., and Capelli, G.M. 1986. Long-term dynamics of three crayfish species in Trout lake, Wisconsin. Can. J. Fish. Aquat. Sci. 43: 993-998.

    Lysne, S.J., Perez, K.E., Brown, K.M., Minton, R.L., and Sides, J.D. 2008. A review of freshwater gastropod conservation: challenges and opportunities. J. N. Am. Benthol. Soc. 27: 463-470.

    MacRae, P.S.D., and Jackson, D.A. 2001. The influence of smallmouth bass (Micropterus dolomeiui) predation and habitat complexity on the structure of littoral zone fish assemblages. Can. J. Fish. Aquat. Sci. 58:342–351.

    10

  • Magurran, A.E. 2009. Threats to freshwater fish. Science. 325: 1215-1216.

    Malley, D.F., and Chang, P.S.S. 1985. Effects of aluminum and acid on calcium uptake by the crayfish Orconectes virilis. Arch. Environ. Contam. Toxicol. 14: 739-747.

    Master, L.L. 1991. Assessing threats and setting priorities for conservation. Conservat. Biol. 5: 559-563.

    Molot, L.A., and Dillon, P.J. 2008. Long-term trends in catchment export and lake concentrations of base cations in the Dorset study area, central Ontario. Can. J. Fish. Aquat. Sci. 65: 809-820.

    Momot, W.T. 1995. Redefining the role of crayfish in aquatic ecosystems. Rev. Fish. Sci. 3(1): 33-63.

    Momot, W.T., Gowing, H., and Jones, P.D. 1978. The dynamics of crayfish and their role in ecosystems. Am. Midl. Nat. 99: 10-35.

    Moore, J.W., Schindler, D.E., Scheuerell, M.D., Smith, D., and Frodge, J. 2003. Lake eutrophication at the urban fringe, Seattle region, USA. Ambio 32: 13-18.

    Myers, N., Mittermeier, R.A., Mittermeier, da Fonseca, G.A.B., and Kent, J. 2000. Biodiversity hotspots for conservation priorities. Nature 403: 853-858.

    Mykra, H., Heino, J., and Muotka, T. 2007. Scale-related patterns in the spatial and environmental components of stream macroinvertebrate assemblage variation. Global Ecol. Biogeogr. 16: 149-159.

    Nystrom, P., Stenroth, P., Holmqvist, N., Berglund, O., Larsson, P., and Graneli, W. 2006. Crayfish in lakes and streams: individual and population responses to predation, productivity and substratum availability. Freshwat. Biol. 51: 2096-113.

    Olden, J.D., McCarthy, J.M., Maxted, J.T., Vetzer, W.W., and Vander Zanden, M.J. 2006. The rapid spread of rusty crayfish (Orconectes rusticus) with observations on native crayfish declines in Wisconsin (U.S.A.) over the past 130 years. Biol. Inv. 8: 1621-1628.

    Olden, J.D., Vander Zanden, M.J., and Johnson, P.T.J. 2011. Assessing ecosystem vulnerability to invasive rusty crayfish (Orconectes rusticus). Ecol. App. 21: 2587-2599.

    Omerod, J.S., Dobson, M., Hildrew, A.G., and Townsend, C.R. 2010.Multiple stressors in freshwater ecosystems. Freshwat. Biol. 55 (Suppl. 1): 1-4.

    Rands, M.R.W., Adams, W.M., Bennun, L., Butchart, S.H.M., Clements, A., Coomes, D., Entwistle, A., Hodge, I., Kapos, V., Scharlemann, J.P.W., Sutherland, W.J., and Vira, B. 2010. Biodiversity conservation: challenges beyond 2010. Science 329: 1298-1303.

    Reid, R.A., and David, S.M. 1990. Crayfish distribution and species composition in Muskoka and Haliburton lakes. Ontario Ministry of the Environment, Dorset, ON, ISBN 0-7729-6560-9, 71 pp.

    Revenga, C., Brunner, J., Henninger, N., Kassem, K., and Payne, R. 2000. Pilot analysis of global ecosystems: freshwater ecosystems. World Resources Institute, Washington D.C.

    Ricciardi, A., and Rasmussen, J.B. 1999. Extinction rates of North American freshwater fauna. Conservat. Biol. 13: 1220-1222.

    11

  • Rukke, N.A. 2002. Effects of low calcium concentrations on two common freshwater crustaceans, Gammarus lacustris and Astacus astacus. Funct. Ecol. 16: 357-66.

    Schindler, D. 2011.The cumulative effects of climate warming and other human stresses on Canadian freshwaters in the new millennium. Can. J. Fish. Aquat. Sci. 58: 18-29.

    Schulz, H.K., Smietana, P., and Schulz, R. 2006. Estimating the human impact on populations of the endangered noble crayfish (Atacus astacus L.) in north-western poland. Aquatic Conserv.: Mar. Freshw. Ecosyst. 16: 223-33.

    Seiler, S.M., and Turner, A.M. 2004. Growth and population size of crayfish in headwater streams: individual- and higher-level consequences of acidification. Freshwat. Biol. 49: 870-881.

    Sharma, S., and Jackson, D.A. 2008. Predicting smallmouth bass (Micropterus dolomieu) occurrence across North America under climate change: a comparison of statistical approaches. Can. J. Fish. Aquat. Sci. 65: 471-481.

    Simberloff, D. 2004. Community ecology: is it time to move on? Am. Nat. 163: 787-799.

    Smith, C.L., and Powell, C.R. 1971. The summer fish communities of Brier Creek, Marshall County, Oklahoma. Am. Mus. Novit. 2458: 1-30.

    Smith, T.M., and Smith, R.L. 2006. Elements of ecology, 6th ed. Benjamin Cummings, San Francisco, USA.

    Somers, K.M., and Green, R.H. 1993. Seasonal patterns in trap catches of the crayfish Cambarus bartonii and Orconectes virilis in six south-central Ontario lakes. Can. J. Zool. 71: 1136-1145.

    Somers, K.M., Reid, R.A., Davies, S.M., and Ingram, R. 1996. Are the relative abundances of orconectid crayfish better indicators of water-quality changes than cambarid abundances? Freshwat. Cray. 11: 249-265.

    Stein, R.A. 1977. Selective predation, optimal foraging and the predator-prey interaction between fish and crayfish. Ecology 58: 1237-1253.

    Stoddard, J.L., Jeffries, D.S., Lukewille, A., Clair, T.A., Dillon, P.J., Driscoll, C.T., Forsius, M., Johannessen, M., Kahl, J.S., Kellogg, J.H., et al. 1999. Regional trends in aquatic recovery from acidification in North America and Europe. Nature 401: 575-578.

    Stuart, S.N., Chanson, J.S., Cox, N.A., Young, B.E., Rodrigues, A.S.L., Fischman, D.L., and Waller, R.W. 2004. Status and trends of amphibian declines and extinctions worldwide. Science 306: 1783–1786.

    Taylor, C.A., Warren, M.L., Fitzpatrick, J.F., Hobbs, H.H., Jezerinac, R.F., Pflieger, W.L., and Robison, H.W. 1996. Conservation status of crayfishes of the United States and Canada. Fisheries 21(4): 25–38.

    Taylor, C.A., Schuster, G.A., Cooper, J.E., DiStefano, R.J., Eversole, A.G., Hamr, P., Hobbs, H.H., Robison, H.W., Skelton, C.E., and Thoma, R.F. 2007. A reassessment of the conservation status of crayfishes of the United States and Canada after 10+ years of increased awareness. Fisheries 32(8): 372–389.

    Taylor, M.F.J., Suckling, K.F., and Rachlinski, J.J. 2005. The effectiveness of the endangered species act: a quantitative analysis. BioScience 55: 360–367.

    12

  • Tonn, W.M. 1990. Climate change and fish communities: a conceptual framework. Trans. Am. Fish. Soc. 119: 337-352.

    Vander Zanden, M.J., Olden, J.D., Thorne, J.H., and Mandrak, N.E. 2004. Predicting occurrences and impacts of smallmouth bass introductions in north temperate lakes. Ecol. App. 14(1): 132-148.

    Venter, O., Broderu, N.N., Nemiroff, L., Belland, B., Dolinsek, I.J., and Grant, J.W.A. 2006. Threats to endangered species in Canada. BioScience 56: 903-910.

    Watmough, S.A., and Dillon, P.J. 2003. Base cation and nitrogen budgets for seven forested catchments in central Ontario, 1983-1999. Forest Ecology and Management 177: 155-177.

    Watmough, S.A., and Aherne, J. 2008. Estimating calcium weathering rates and future lake calcium concentrations in the Muskoka-Haliburton region of Ontario. Can. J. Fish. Aquat. Sci. 65: 821-833.

    Wilcove, D.S., Rothstein, D., Dubow, J., Phillips, A., and Losos, E. 1998. Quantifying threats to imperiled species in the United States. BioSci. 48: 607-615.

    Williams, J.E., Johnson, J.E., Hendrickson, D.A., Contreras-Balderas, W., Williams, J.D., Navarro-Mendoza, M., McAllister, D.E., and Deacon, J.E. 1989. Fishes of North America endangered, threatened, or of special concern: 1989. Fisheries 14: 2-20.

    Wilson, K.A., Magnuson, J.J., Lodge, D.M., Hill, A.M., Kratz, T.K., Perry, W.L., and Willis, T.V. 2004. A long-term rusty crayfish (Orconectes rusticus) invasion: dispersal patterns and community change in a north temperate lake. Can. J. Fish. Aquat. Sci. 61: 2255–2266.

    Wright, D.A. 1995. Trace metal and major ion interactions in aquatic animals. Mar. Poll. Bull. 31: 8-18.

    13

  • Chapter 2 Multispecies crayfish declines in lakes: implications for species

    distributions and richness

    2.1 Abstract Aquatic communities are highly threatened by anthropogenic and climate changes. However,

    despite their importance in these communities, information regarding temporal changes in

    populations and assemblages of North American crayfish is scarce. Long-term monitoring of

    crayfish populations in south-central Ontario, Canada, indicates that the populations are in a

    significant state of decline. We sought to determine whether these population declines are

    spatially and taxonomically broad, and if so, what factors might be associated with the declines.

    We sampled crayfish abundance (catch per unit effort) in 100 lakes, and compared current

    abundances to survey results from the early 1990s. Abundances of all species (natives and

    nonnatives) declined significantly during this interval. Declines were both severe (63– 96% loss

    of abundance) and geographically widespread for all species. Previous studies have documented

    native species declines caused by the invasive crayfish Orconectes rusticus, but this species was

    absent from almost all lakes and was not a factor in the declines. We hypothesize that the

    introduction of predatory smallmouth bass (Micropterus dolomieui), increases in Al

    concentrations, and reduced Ca concentrations in these lakes are negatively affecting crayfish

    populations.

    2.2 Introduction Aquatic ecosystems are severely threatened by environmental change and loss of biodiversity. In

    North America, the number of aquatic taxa in need of conservation or monitoring vastly

    outnumbers the number of terrestrial taxa of the same status (Master 1991). Literature on the

    status of North American freshwater fishes (e.g., Williams et al. 1989, Jelks et al. 2008) and

    amphibians (reviewed in Stuart et al. 2004) has mounted during the past 20y, but North

    American crayfish have received less attention (Taylor et al. 1996, 2007) despite their

    importance in aquatic ecosystems (Momot et al. 1978). Information on the status of crayfish in

    Canada is even more limited (Hamr 1998, 2006).

    14

  • Ontario has the richest crayfish biodiversity in Canada and is home to 9 of the 11 species that can

    be found nationwide. These species include natives (Fallicambarus fodiens, Cambarus diogenes,

    C. bartonii, C. robustus, Orconectes immunis, O. propinquus, and O. virilis) and nonnatives (O.

    obscurus and O. rusticus). Work has begun on determining the status of crayfish in southern

    Ontario, particularly in relation to the burrowing crayfishes C. diogenes and F. fodiens (Hamr

    2006, Guiasu 2007), but crayfish status elsewhere in Canada has not been directly evaluated. The

    most recent status report of the Canadian Endangered Species Conservation Council (CESCC

    2006; www. wildspecies.ca) lists no native species as ‘‘At Risk’’ or ‘‘May be At Risk.’’ The

    burrowing crayfishes C. diogenes and F. fodiens are listed as ‘‘Sensitive,’’ whereas the

    remaining native species are listed as ‘‘Secure.’’ However, this ranking has been based on very

    sparse monitoring efforts, particularly in central and northern Ontario. In fact, several native

    populations in lakes in south-central Ontario appear to have experienced significant declines

    (David et al. 1994) that might indicate broader ecological issues.

    The general consensus is that 4 major causes of aquatic imperilment exist: 1) loss or degradation

    of appropriate habitat, 2) various forms of chemical pollution, 3) introductions of nonnative

    species, and 4) overexploitation for human uses (Allan and Flecker 1993, Wilcove et al. 1998).

    In the case of crayfish, overexploitation for human uses is not a likely factor. Reason exists to

    hypothesize that any of the other 3 factors might be affecting crayfish, but to date, no studies

    have examined the broader status of crayfish populations and communities. In general, crayfish

    community structure is not well understood, and few data exist with which to assess particular

    trends in crayfish communities.

    Crayfish are the largest freshwater crustaceans in North America and where present, they often

    comprise a large portion of the total biomass in the ecosystem (Momot et al. 1978). Crayfish are

    omnivores, and can act as primary consumers, carnivores, and decomposers (Momot 1995, Dorn

    and Wojdak 2004). Thus, they are an important component of aquatic food webs and transfer

    energy from lower to higher trophic levels when they are consumed by predatory fishes,

    mammals, and birds. Systems without crayfish have diminished energy cycling, community

    productivity, and food availability at the top of the food chain. Thus, crayfish might be keystone

    species where they are present (Momot 1995). Crayfish are ecosystem engineers. They modify

    the physical environments in which they live and alter breakdown and availability of basal food

    15

  • sources (Creed and Reed 2004). Thus, changes to crayfish communities could have broad effects

    in aquatic ecosystems.

    Our objective was to determine the current status of crayfish populations across south-central

    Ontario (>22,000 km2), and if changes were detected, to determine whether particular

    environmental factors might be contributing to these changes. We compared crayfish abundances

    and water chemistry data from 100 lakes to survey results from the early 1990s (David et al.

    1997, Ontario Ministry of Environment [MOE], unpublished data) to assess changes. We

    evaluated the community-level and distributional implications of any population changes

    detected and determined environmental factors that might be related to the patterns observed in

    the abundances of crayfish in these lakes.

    2.2.1 Study Lakes and Study Region

    Our survey included 100 inland lakes from 9 tertiary watersheds across south-central Ontario

    (Fig. 1), based on the availability of historical records for crayfish and water chemistry. The

    lakes range in longitude from 78.239°W (Kawartha region) to 81.039°W (Georgian Bay region),

    range in latitude from 44.109°N (Scugog region) to 46.269°N (Sudbury area), and cover a wide

    geographical range (minimum convex polygon area of 22,300 km2).

    Most of the lakes were in 4 tertiary watersheds: Georgian Bay Tributaries (2EA), Moon and Go

    Home rivers (2EB), Severn River (2EC), and the Cameron Lake Drainage (2HF). The geology of

    this region is typical of the Canadian Precambrian Shield, with a predominance of granitic

    bedrock and pockets of thin, acidic, and nutrient-limited soils (Jeffries and Snyder 1983,

    Chapman and Putnam 1984). Secondary-growth, mixed forest covers much of the study area,

    with patches of coniferous- and deciduous-dominated stands distributed throughout the forest

    (David et al. 1997). These watersheds are characterized by different intensities of cottage

    development and recreational use and include a number of small communities.

    Eight more northern Shield lakes were from the Sudbury region (2CF) and from Algonquin Park

    (Upper Madawaska River [2KD] and Deep [2KB] watersheds and the northeastern corner of the

    Moon and Go Home River watershed [2EB]). The Sudbury region is sparsely vegetated with

    secondary-growth mixed forest (Girard et al. 2006). This area of Algonquin Park is dominated by

    coniferous forest and is completely undeveloped (except for walking trails and camp sites) where

    16

  • the study lakes were situated. Four lakes were south of the Shield and enabled us to compare and

    contrast crayfish populations and physicochemical variables between the 2 geological regions.

    The 4 off-Shield lakes (1 in the southern tip of tertiary watershed 2HF and 3 in watersheds 2HH

    and 2HG) are in heavily urbanized and deforested areas, experience high levels of recreational

    use year-round, and are hard-water lakes that are rich in Ca. Collectively, the Shield lakes and

    the southerly off-Shield lakes represented a long gradient of anthropogenic impacts, including

    atmospheric acidification and metal deposition, and human development intensity.

    Figure 2-1. Study region in Ontario, Canada, showing the 100 lakes surveyed. Tertiary watersheds are delineated and identified by the following codes: 2EA = Georgian Bay tributaries, 2EB = Moon and Go Home rivers, 2EC = Severn River, 2HF = Cameron Lake drainage, 2CF = Sudbury Region, 2KD = Upper Madawaska River, 2KB = Deep River, 2HH = Kawartha Lakes region, 2HG = Scugog River.

    17

  • 2.3 Methods

    2.3.1 Site selection and crayfish sampling

    Site selection and sampling methods were developed by the MOE (David et al. 1994). Recently

    molted individuals, berried females, or females carrying young rarely enter traps (Somers and

    Green 1993, Richards et al. 1996). Moreover, crayfish are most active, and thus, most likely to

    enter traps, when surface water temperatures are >20°C (Somers and Green 1993, Richards et al.

    1996, Hein et al. 2007). Therefore, each lake was sampled once between late June and the end of

    August to coincide with the period of highest crayfish catchability when both cambarid and

    orconectid crayfishes should be in an intermolt stage, females should not be carrying young

    (Crocker and Barr 1968, Somers and Green 1993, David et al. 1994, Richards et al. 1996, but see

    Hamr and Berrill 1985), and when water temperatures had reached 20°C. This limited

    catchability window constrained sampling such that most lakes were sampled over 3 summers

    (2005–2007). Five lakes were part of MOE’s regular crayfish population monitoring program

    and had been sampled in 2002 to 2004 (MOE, unpublished data). The historical data were

    collected over 6 summers (1989–1992, 1994, 1995).

    Crayfish were collected with standard, commercially available, wire-mesh Gee minnow traps.

    Each trap was baited with a single perforated plastic film canister (5cm tall, 3cm diameter) filled

    with fish-flavored canned cat food. Funnel entrances were enlarged to 3.5-cm diameter to

    accommodate larger crayfish. Traps were set and then retrieved the following day (18–26 h later)

    so that traps were in place at night when crayfish are most active.

    Three site types (rock, macrophyte, or woody debris dominated) were sampled in each lake

    because species vary in terms of their preferred habitats (Crocker and Barr 1968, Nystrom et al.

    2006). Fifty- four traps were set in each lake (18 traps at each of the 3 site types). Three trap

    lines, each consisting of 6 traps secured at 3-m intervals, were set perpendicular to the shore 2 to

    5 m apart at locations with a minimum depth of 0.5 m for the first trap in a line and a place on

    the shoreline where the line could be tied. Trap depths ranged from 0.5 to 8 m depending on the

    slope of the littoral zone. This design is similar to that used to collect the historical data, in which

    trap depths ranged from 1 to 6 m in depth at 1-m depth intervals (David et al. 1997). Single

    baited traps effectively sample a radius of 4.2 m (56.3 m2, Acosta and Perry 2000). Therefore,

    the total area sampled by the historical and current sampling designs is equivalent. Crayfish were

    18

  • identified using the taxonomic keys in Crocker and Barr (1968). The number of crayfish/species

    in each trap was used to calculate a catch per unit effort (CPUE) estimate of relative abundance.

    2.3.2 Chemistry sampling

    Water chemistry was sampled in the same year that crayfish were sampled in early spring before

    lakes became stratified. Epilimnetic water was collected using a 5-m vertical composite sampler

    (Girard et al. 2007). Access to a small number of lakes was difficult in spring because of road

    washouts, so water samples from these lakes were collected with the same apparatus but in

    summer when crayfish were sampled. In deeper lakes, this sampling approach represents the

    chemical conditions of only the epilimnion, but this approach is appropriate because it matches

    that method used by David et al. (1997) and because crayfish preferentially inhabit this depth

    (Jones and Momot 1981).

    A total of 18 chemical variables (pH, alkalinity [mgL-1], conductivity [mScm-1], Al, Mn, and

    Fe [μgL-1], dissolved inorganic and organic C [DIC and DOC, respectively; mgL-1], Mg, Ca,

    K, Na, Cl, and SO4 [mgL-1], and NH4, NO3, total Kjeldahl N, and total P [μgL-1]) were

    analyzed from these samples by the Ontario Ministry of the Environment, using standard

    analytical methods and quality assurance/quality control procedures (Anonymous 1983).

    Accidental freezing in the laboratory resulted in the loss of 35 DIC samples in the current survey,

    and 6 DIC samples were lost for unreported reasons in the historical study. These losses reduced

    the number of lakes for which the comparison of DIC was possible to 60 (Scugog Lake was the

    only off-Shield lake retained). A linear regression model relating Cl to Na was used to estimate

    the historical Na concentration for Scugog Lake.

    2.3.3 Data analysis

    Model II major axis regression was used to examine the congruence between current and

    historical CPUE for each species. Model II regressions are appropriate when both variables are

    subject to error (from natural inherent variability or measurement error; Chen and Jackson 2000),

    and allowed us to determine the slope and y-intercept of the interrelationship between 2 variables

    when we were not interested in the independent and dependent (i.e., predictor and response)

    relationship between them (Sokal and Rohlf 1995). If no changes had occurred between the 2

    survey periods, one would expect a strong regression relationship with slope = 1. This

    19

  • expectation was evaluated with t-tests to determine whether the modeled slopes differed

    significantly from the null expectation of a 1:1 relationship. The t-tests were based on the

    formula, t = (b1 - 1)/SEb1, where b1 is the slope of the major (Model II) axis and SEb1 is its

    standard error (see Yang et al. 2004).

    To evaluate changes at the community level, a frequency distribution of the number of lakes with

    0, 1, 2, 3, and 4 species was generated for both the historical and current data sets. Fisher’s exact

    test was used to determine whether these species richness relationships had changed significantly

    between the 2 survey periods.

    Paired t-tests were used to screen chemical variables for significant changes between current and

    historical conditions in all lakes and then in only Shield lakes. Tests were corrected for multiple

    comparisons with the False Discovery Rate approach (Benjamini and Hochberg 1995). This

    correction technique is particularly appropriate when conducting exploratory analyses or when

    the variables under consideration covary (reviewed in de Castro and Singer 2006). Each variable

    that showed a significant change was further analyzed with Model II regression to obtain a visual

    assessment of the trends between the 2 surveys, again with the 1:1 line as the baseline

    expectation.

    Table 2-1. Results of the model II regression analyses comparing current and historical relative abundances (Catch Per Unit Effort [CPUE]) for all lakes in which a species was found. n = the number of lakes in which a species was found, p = probability associated with the difference from the null expectation (1:1), % historical = the percentage of lakes in which the species occurred historically that have current populations of the species.

    Species n r SE Slope p % historical

    O. virilis 57 0.61 0.044 0.28

  • 2.4 Results

    2.4.1 Crayfish

    2.4.1.1 Abundance

    Seven crayfish species (O. immunis, O. obscurus, O. propinquus, O. rusticus, O. virilis, C.

    bartonii, and C. robustus) were encountered during both studies. Crayfish were not found in 25

    lakes during the historical survey and in 33 lakes during our survey. Where crayfish were found,

    total crayfish abundance (as CPUE) including all species present ranged from 0.01 to 12.8 in the

    historical survey and from 0.02 (in 8 lakes) to 2.89 in our survey.

    Abundances of all species decreased between the 2 surveys. Slopes of all lines generated by

    Model II regression analyses were significantly

  • Figure 2-2. Model II regression plots for current vs historical abundance (as catch per unit effort [CPUE]) of Orconectes virilis (A), O. propinquus (B), O. immunis (C), O. obscurus (D), Cambarus bartonii (E), and C. robustus (F), in relation to the 1:1 null expectation (dashed line). Insets show details for species with many low abundances.

    22

  • 2.4.1.2 Species richness

    Species richness was distinctly lower in our survey than in the historical survey, but the shift was

    not statistically significant (Fisher’s exact test, p = 0.069; Fig. 3). The percentage of lakes with

    no crayfish increased from 25 to 33%, and the modal species richness decreased from 2 (32% of

    lakes) to 1 (38% of lakes) (Fig. 3). In the historical survey, 53% of lakes contained ≤1 species

    and numerous lakes contained 3 or 4 species, whereas in our survey, 71% of lakes contained ≤1

    species and none were found to continue supporting 4 species.

    0

    5

    10

    15

    20

    25

    30

    35

    40

    0 1 2 3 4Number of species

    Num

    ber o

    f lak

    es

    Historical

    Current

    Figure 2-3. Frequency distributions of crayfish species richness in the historical and current surveys.

    2.4.1.3 Distribution

    The number of lakes inhabited by each species has decreased for all species except O. immunis

    (Fig. 4). The orconectids tended to have fewer apparent losses and less serious declines than did

    the cambarids. Orconectes immunis appears to have been lost from 2 lakes (40.0% of historical

    occurrences) and was newly detected in 4 lakes (80.0%). Orconectes propinquus appears to have

    been lost from 10 lakes (28.6%) and has declined by ≥50% in 10 lakes (28.6%) (Fig. 5A). In

    total, 57.1% of O. propinquus populations are currently at risk or have been lost, but these losses

    were partially offset by 4 new detections (11.4%). No obvious spatial patterns in O. propinquus

    23

  • losses or detections were observed (Fig. 5A), although 3 losses occurred in the lakes in the Black

    River system at the northern tip of the Severn River Watershed (2EC). Orconectes virilis appears

    to have been lost from 16 lakes (34.0%) and has declined ≥50% in 15 lakes (31.9%) (Fig. 5B). In

    total, 66.0% of O. virilis populations are currently at risk or have been lost, but these losses were

    offset by 10 new detections (21.3%). A large number of O. virilis population losses or reductions

    occurred in one set of connected lakes in the Black River system, whereas O. virilis was newly

    detected in each of a string of 4 connected lakes in the northwestern portion of the Cameron

    Lake Drainage (2HF) (Fig. 5B).

    Figure 2-4. Changes in the number of lakes with populations of Orconectes virilis (O.v.), O. propinquus (O.p.), O. immunis (O.i.), O. obscurus (O.o.), O. rusticus (O.r.), Cambarus bartonii (C.b.), and C. robustus (C.r.), between the historical and current surveys in relation to the 1:1 null expectation (dashed line).

    The apparent loss of populations was most marked for the 2 cambarid species (Fig. 4). Cambarus

    bartonii appears to have been lost from 19 lakes (59.4%) and has declined by ≥50% in 7 lakes

    (21.9%) (Fig. 5C). In total, 81.3% of C. bartonii populations have been lost or are at risk, and

    these losses were offset by only 2 new detections (6.3%). Cambarus bartonii losses and declines

    have occurred across the northern and southern portions of its historical range, but a narrow band

    of currently stable populations was found across the center of the range. Cambarus robustus

    24

  • appears to have been lost from 6 lakes (54.5%) and has declined substantially in 1 lake (9.1%)

    (Fig. 5D). These results indicate that 63.6% of C. robustus populations are currently at risk or

    have been lost, and these losses were not offset by new detections. Cambarus robustus appears

    to have been lost in all of its southern and eastern historical range and is now limited to a small

    segment of the northern tip of a single watershed, the Georgian Bay tributaries (2EA).

    Figure 2-5. Distributions of Orconectes propinquus (A), O. virilis (B), Cambarus bartonii (C), and C. robustus (D), indicating populations that appear stable, have declined by ≥50%, appear to have been lost, or were newly detected.

    25

  • 2.4.2 Water chemistry

    Significant changes between the historical and current chemical conditions were detected for 9

    variables (Table 2). Mean alkalinity, Al, Cl, Na, and NO3 increased significantly (by ~16, 76, 33,

    45, and 132%, respectively), whereas mean SO4 decreased significantly (~25%) between

    surveys. However, alkalinity did not differ significantly between surveys when off-Shield lakes

    were omitted from the analysis. Temporal trends in the remaining variables differed between

    lakes on and off the Canadian Shield. Mean Ca and Mg decreased significantly (10%) between

    surveys in Shield lakes but increased in off-Shield lakes. In contrast, DIC increased significantly

    (16%) in most Shield lakes for which data were available but decreased in off-Shield Lake

    Scugog. Comparisons at the watershed level on the Shield were generally consistent with these

    findings, however not all watersheds showed a significant change in every variable (Table S1).

    Table 2-2. Chemical variables that changed significantly in all study lakes or in the Shield lakes between the historical survey and the current study. Δ = % change, Alkti = alkalinity, DIC = dissolve inorganic C, p = probability associated with paired t-tests comparing current and historical values, * indicates differences were significant only in Shield lakes and means and Δ apply only to Shield lakes, ns = not significant (p > 0.05).

    Parameter Current Historical Δ % All Lakes Shield Lakes

    Alkti (mg·L-1) 8.22 7.09 16.03 0.0102 NS

    Al (μg·L-1) 52.30 29.70 76.09

  • Model II regression results (Fig. 6A–I) provide support for the differences detected by paired t-

    tests; however, 3 cases warrant cautious interpretation. Present and historical values of alkalinity

    were strongly correlated (r = 0.91; Fig 6A). However, values declined slightly in a large number

    of lakes and increased strongly in a few lakes with historically low concentrations. These few

    lakes with large increases might have influenced the results of the paired t-test. The increase in

    Al was well supported (r = 0.63; Fig. 6B), but Al decreased in a large number of lakes. NO3

    increased dramatically in many lakes, but the pattern of increases was highly variable (r = 0.25;

    Fig. 6H) and the regression was driven by increases in lakes with historically low NO3

    concentrations.

    27

  • Figure 2-6. Model II regression plots for log(x) transformed current vs historic


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