swimmers itch drivers in northern mi lakesplattelake.org/resources/documents/member info/2017...
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Swimmers itch drivers in northern MI lakes
Thomas R. Raffel, Ph.D.
Department of Biological Sciences
Oakland University
Rochester, MI
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Schistosomiasis:• 2-host life cycle (SNAILS)
• Exposure in water
• Human schistosomes (3 spp)• 2nd most important tropical disease worldwide
• 200-300 million people infected/yr; 800,000 deaths
• Avian schistosomes (12-15 spp)• Trying to infect birds
• Itchy bumps 1-2 days post-exposure
• Gradually fade over ~1 week
Adult worms (in blood vessel)
Trichobilharzia cercariapenetrating skin
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• Trichobilharzia spp.• First described by Cort in
Douglas Lake (1928 )
Michigan: home of swimmer’s itch!
Physa integra
Stagnicola catescopium* (= Stagnicola emarginata)
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Research Goals
1. Temporal dynamics
• Generate daily field data for cercaria abundance
• Test predictions for potential warning systems
2. Spatial distribution
• Identify landscape-level predictors of snail and parasite abundance
• Inform management decisions
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• High day to day variation reported, but no daily
field data available for cercaria abundance
• Trematode biology is temperature-dependent
- Snail growth & reproductive rates
- Cercaria production rate
• Most studies ignore temperature fluctuations
I. Temporal dynamics: Gaps in Knowledge
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6/1 6/8 6/15 6/22 6/29 7/6 7/13 7/20 7/27
Tem
per
ature
, C
elsi
us
Date
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Thermal Stress Hypothesis (Paull et al 2015)
• Proposed that high temperatures are energetically stressful to snails, depleting energy stores (e.g., fat reserves) during long warm periods.
• Depleted host energy limits cercaria production by trematode parasites
I. Temporal dynamics:
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I. Temporal dynamics: Thermal Stress Hypothesis
Warm
Temperatures
Metabolism
(reaction rates)
Energy budget of
snail (fat reserve)
Cercaria
Immediate Effect
Delayed Effect
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Higher levels when currentwater temperature is high
Lower levels following
multiple days of warm
temperatures
I. Temporal dynamics: Thermal Stress Hypothesis
Predictions:
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Summer 2015 – Madelyn Messner
• Needed a large number of daily cercaria samples from
natural sites during peak swimmer’s itch season
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Citizen scientists!
• Volunteer recruitment & training
• Daily samples: July 6 – August 2
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Temporal dynamics: July 6 – August 2, 2015
Daily samples- filter
50L water
Hourly temperature
& light
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Sample ProcessingCollect filter sample
Extract DNA
qPCR to estimate
cercaria abundance
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• 378 individual sample tubes
• DNA extraction from dried sample
− 1 mL lysis buffer + 10 uL proteinase K
• qPCR – DNA quantification
− TaqMan Assay (Jothikumar et al 2015)
− Target itch-causing schistosomes
− Singlicate reactions w/reruns for inhibited reactions
IPC measures reaction inhibition (reduces measurement bias)
Singlicate reactions (low precision for individual measurements)
Temporal dynamics: sample processing
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Temporal dynamics: statistical analysis
Response variable:
Cercaria/ 50L
Substantial day to day
variation
Random effects:
- Location
- Snail population
- Snail infection levels
- Bird visitation
- Water currents
Log cercaria/ 50L
Min Daily Temp
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EXAMPLE: (Hypothetical)
• Pirate attacks correlate
with ocean wind speed
• Can we conclude increased
wind speed caused the
increase in pirate attacks
through time?
Temporal dynamics: temporal confoundment
YEAR17901755 1780 17851750
Pir
ate
atta
cks
Ocean
win
d sp
eed
Problem:
• THOUSANDS of possibly relevant variables increased or decreased during this time period, making this a potentially CONFOUNDED predictor variable
Poor evidence for causality (temporally confounded analysis)
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Standard method – account for
long-term trend first, before
testing for relationships
Method 1:
• “Detrend” cercaria data
using deviations from a
spline curve fit to data
Temporal dynamics: temporal confoundment
*Method 2:
• Use past cercaria levels (over 3, 5, or 7 days) as a covariate in the
analysis. Past levels predict current levels.
AFTER accounting for the long-term trend, we tested for effects of current & past daily temperatures on cercaria abundance
Better evidence for a meaningful relationship
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Random variation…. (singlicate analyses)
Best model according to AIC: 3 predictors
1. Higher cercaria levels in past 5 days →
higher cercaria levels today
2. Current temps positive trend
3. Past temps significant negative effect
Predictor variable Coefficient χ2 p-value
Log cercaria prev 5 days 1.94 23.9 <0.001
Min daily water temp 0.24 2.66 0.10
Previous 5 day water temp -0.69 14.0 <0.001
Temporal dynamics: Results
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Temporal dynamics: Conclusions
• Field evidence for
Thermal Stress Hypothesis
• Positive effect of current temps
- Widely cited in literature
- Weaker (non-significant) effect in our analysis
Negative effect of past temps
- Novel finding; highly significant and predictive
- Higher-precision assays might help improve predictions in the future
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Research Goals
1. Temporal dynamics
• Generate daily field data for cercaria abundance
• Test predictions for potential warning systems
2. Spatial distribution
• Identify landscape-level predictors of snail and parasite abundance
• Inform management decisions
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II. Large-Scale Spatial Survey (16 lakes; 38 sites)
Maddie&
Jenna
Jason&
Ryan
Aleena & Alex
• >50 volunteers trained• >1040 cercaria samples collected• >3000 miles driven• >2500 qPCR assays run
What determines patterns of schistosome cercariaeabundance across a broad landscape?
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What determines swimmer’s itch at a particular SITE?
Snail population density
Percent snails infected
Cercariae produced per snail
Bird infection?
Temperature? Algal
growth?
Cercariaein water
SWIMMER’S ITCH!
Wind/Waves?
Possible environmental drivers…..
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Land Use • Urbanization• Agriculture• Vegetation• Development
Physical charateristics• Wave action• Lake size/depth• Substrate type• Temperature
Cercariae in water
Herbicide runoff
Zebra mussels
Insecticide runoff
Nutrient pollution (N, P)
Snail density
Arthropod predators (crayfish)
Attached algae
Water clarity
−
−
−Hypothesized drivers:
Bird visitation
Water clarity hypotheses*:
1. Clear water lets light penetrate to bottom of lake2. Algal periphyton is often light-limited, especially in deeper water3. Snail populations are often limited by periphyton (food) abundance 4. Trematode abundance often limited by abundance of host snails
Infected snailsTemperature
−
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Continuous/Daily monitoring:• Cercaria density - daily filtered-water samples (volunteers + qPCR)• Wind speed & direction (volunteers)• Water temperature & light penetration (HOBO loggers)• Bird visitation
Weekly surveys:• Snail quadrat sampling & collection (identification, size distribution)• Turbidity & zebra mussel densities (quadrats)• Crayfish trapping• Zooplankton sampling (density, composition)
Site-level measurements:• Attached algae (periphyton) growth & composition• Zebra mussel settling rates• Water chemistry (nitrates+nitrites+ammonia, organophosphate)• Pesticides (2,4-D; glyphosate)• Sediment cores (Phosphorus, Organic carbon)• Substrate & shoreline characteristics; fetch; slope
Lake-level characteristics:• Land use in watershed & near shore• Lake size & depth
2016 survey parameters (>60 possible predictors….):
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Results Part 1: Snails responded to water clarity
Supported a core prediction of our water clarity hypotheses….
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HOWEVER: Snails were dominated by Pleurocera…
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Pleurocera drove the Turbidity pattern…
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… and Pleurocera are NON-HOST snails.
Characteristics:• Thick-walled shells• Operculate• Common in larger rivers• MI is northern edge of
known distribution
Not known to host Trichobilharzia sp. parasites
Encyclopedia of Life:Pleurocera collection records
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Results 2: Cercariae responded to Stagnicola
• No added predictive power by adding other snail species to the analysis
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Cercaria levels versus Stagnicola density:
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Comparing 2015 & 2016 datasets:
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“Stagnicola” snails:
Encyclopedia of Life:Stagnicola collection records
Characteristics: Known hosts for Trichobilharzia spp.
parasites• Non-Operculate• ARCTIC taxon – rare south of MI• Eat algal periphyton & macrophytes• Lives in deep water (up to 30 feet for
L. catascopium)• Prefer solid substrates• Regulation by fish predators…?
“Stagnicola” snails:
Stagnicolacatascopium/emarginata/elodes
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“Stagnicola” snails:
Stagnicolacatascopium/emarginata/elodes
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Some sites had cercariae despite no Stagnicola….
• Might indicate influx of cercariae from offsite via water currents
• Can we account for any of this variation in our analysis?
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F1,35 = 7.0; P = 0.012
Sites with few or no Stagnicola snails
How could submerged vegetation reduce the influx of cercariae from other sites?
Results 3: Submerged vegetation reduced cercariae(after accounting for snail density)
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Plants as physical barriers? Plants as accidental “hosts”?
Hedychia coronarium (mariposa)(Warren & Peters 1968)
Floating water plants(Christensen 1979)
How could submerged vegetation reduce the influx of cercariae from other sites?
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Bladderwort (Utricularia spp.)
• Carnivorous water plant• Known to eat cercariae!• Widespread in MI• Sometimes mistaken for milfoil
Eurasian milfoilBladderwort
Gibson & Warren 1970
Cercariae
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Cercariae
Submerged vegetation Stagnicola
Maximum Lake Depth
Deciduous trees
−
Summary – Swimmer’s itch apparent risk factors
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Shallow Lake:
Deep Lake:
HIGH Risk
LOW Risk Medium Risk
Medium Risk
Summary – Swimmer’s itch apparent risk factors
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THANK YOU!!!
Funds & Lodging (still compiling names for 2016…):
RAFFEL LAB:Madelyn Messner*Jason Sckrabulis*Ryan McWhinnie*Jenna McBride*Alex BagerisAleena HajekKarie Altman
Collaborators:Pieter Johnson, Sara Paull, Bryan LaFonte, Curt Blankespoor, Ronald Reimink, David Szlag
Oakland University Support:Doug Wendell (chair), Arik Dvir, Cathy Starnes, Sheryl Hugger, Jan Bills, Kathy Lesich, Shawn Rasanen
Oakland Undergraduate researchers:Fieldwork: R. McWhinnie, J. McBride, A. Hajek, A. Bageris; qPCR: J. McBride, S. Trotter, G. Everett, J. Willis; Invertebrate counts: Melissa Ostrowski, James Willis, Rima Stepanian, Aman Singh
Oakland University StartupAl Flory & Monika SchultzChimney Corners ResortPlatte Lake Improvement AssnGlen Lake AssociationLake Leelanau Lake AssnLeelanau Clean WaterWalloon Lake AssociationLime Lake AssociationHiggins Lake Property Owners Assn
SICON LLCTwin Lakes Property Owners AssnElk-Skegemog Lake AssnCrystal Lake & Watershed Org.Lake Margrethe Foundation FundHamlin Lake Preservation SocietyPortage Lake Watershed ForeverIntermediate Lake Association
ALL OUR CITIZEN SCIENTIST VOLUNTEERS! (NEXT SLIDE)
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• (Crystal Lake) Al Flory & Monica Schultz; Ted & Barb Fischer; Pat & Sherry Grant• (Glen Lake) Mike & Sara Litch; Rob Karner; John DePuy; John Kassarjian• (Lake Leelanau) John Lutchko; Dave Hunter; John Popa; Wayne Swallow• (Platte Lake) Bob & Mason Blank; Wilfred Swieki• (Little Traverse Lake) Len Allgaier• (Lime Lake) Dean Manikas• (Walloon Lake) Russ Kittleson• (Higgins Lake) Ron Reimink; Curt Blankespoor
• (Crystal Lake) Al Flory & Monica Schultz; Ted Fischer; Jana Way; Joel Buzzell; Shary Grant
• (Deer Lake) Todd Sorenson; Alec Sherman
• (Douglas Lake) Curt Blankespoor; Kira Surber
• (Elk Lake) Bob & Bryce Kingon; Dean Ginther; Ruth Bay
• (Glen Lake) John Kassarjian; Mike Litch; Denny Becker; Bill Meserve; Jack Laitala; Chris Dorsey Shugart
• (Hamlin Lake) Ginny Hluchan; Linda & Ted Leibole; Judi Cartier & Ed Franckowiak; Paula & Mike Veronie; Denny Lavis; Joe
Muzzo; Mara DeChene; Gail Hanna; Kathy Grossenbacher; Jim Gallie
• (Higgins Lake) Jim Vondale; Charlene Cornell; Richard Weadock; John & Susan Osler; Anne Grein; Ken Dennings; Greg Douglas;
Rebekah Gibson; Sue Gederbloom
• (Intermediate Lake) Steve & Kathy Young; Jim & Karen Gilleylen; Scott Zimmerman; Marcia Collins; Claude & Joyce Gilkerson;
Sheridan & Bob Haack
• (Lake Leelanau) David Hunter; John Popa; John Lutchko; Nick Fleezanis; Page Sikes
• (Lime Lake) Dean Manikas
• (Little Traverse Lake) Len Allgaier and Kristin Race
• (Lake Margrethe) Sandra & Ken Michalik; Mike Ravesi; Lisa Jaenicke; Nancy Atchison
• (Platte Lake) Wilfred J. Swiecki; Bob Blank; Tom & Christian Inman; Jackie & John Randall
• (Portage Lake) Al Taylor; Mary Reed; Tammy Messner; Ted Lawrence
• (Lake Skegemog) Dave Hauser; Kathi Gober
• (Walloon Lake) Christine Wedge; Russ & Kathy Kittleson; John Markewitz; Megan Muller-Girard
2015 survey volunteers (8 lakes)
2016 survey volunteers (16 lakes)
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What does thermal stress predict through time?
Cold to Warm: initial increase in parasite production followed by steady decline
Constant Warm: parasite production declines longer it is held at warm temps
Paull et al 2015
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I. Large-Scale Survey (16 lakes; 38 sites)
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Primary drivers of Pleurocera:
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D45L
D90
D45R
Effective Fetch (Lf )
𝐸𝑓𝑓𝑒𝑐𝑡𝑖𝑣𝑒 𝐹𝑒𝑡𝑐ℎ =σ 𝐷𝑖 × 𝑐𝑜𝑠 𝛾𝑖
σ𝑐𝑜𝑠 𝛾𝑖
• Distance wind can blow over water more wave action (in theory)
• Correlates with lake size & depth
𝑀𝑜𝑑𝑖𝑓𝑖𝑒𝑑 𝐸𝑓𝑓𝑒𝑐𝑡𝑖𝑣𝑒 𝐹𝑒𝑡𝑐ℎ =𝐷45𝐿𝑐𝑜𝑠 45° + 𝐷90𝑐𝑜𝑠 90° + 𝐷45𝑅𝑐𝑜𝑠 45°
𝑐𝑜𝑠 45° + 𝑐𝑜𝑠 90° + 𝑐𝑜𝑠 45°
But why are Pleurocerid snails more abundant at high-Fetch sites?
Possible hypothesis:• Adapted for shallow water & high wave action
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Drivers of water clarity:
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Drivers of mussel abundance:
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Conifers – effects on turbidity, snails, & mussels?
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Conifers – effects on turbidity, snails, & mussels?
• Conifers release terpenes (“turpentine”)
Toxic to algae? (few studies)
• Less algae → lower turbidity
Less food for mussels
More food for snails
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D45L
D90
D45R
Water clarity
Pleurocera(Dominant snail)
Fetch
Temperature
Mussels
Alkalinity
Gravel
Conifers −−
Summary – factors affecting snail (Pleurocera) abundance