Swimmers itch drivers in northern MI lakes Thomas R. Raffel, Ph.D. Department of Biological Sciences Oakland University Rochester, MI
Schistosomiasis: • 2-host life cycle (SNAILS) • Exposure in water • Human schistosomes (3 spp) • 2 nd most important tropical disease worldwide • 200-300 million people infected/yr; 800,000 deaths Adult worms • Avian schistosomes (12-15 spp) (in blood vessel) • Trying to infect birds • Itchy bumps 1-2 days post-exposure • Gradually fade over ~1 week Trichobilharzia cercaria penetrating skin
Michigan: home of swimmer’s itch! • Trichobilharzia spp. • First described by Cort in Douglas Lake (1928 ) Stagnicola catescopium * (= Stagnicola emarginata ) Physa integra
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
I. Temporal dynamics: Gaps in Knowledge • 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 26 25 Temperature, Celsius 24 23 22 21 20 19 6/1 6/8 6/15 6/22 6/29 7/6 7/13 7/20 7/27 Date
I. Temporal dynamics: 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: Thermal Stress Hypothesis Warm Temperatures Immediate Effect Metabolism Energy budget of (reaction rates) snail (fat reserve) Delayed Effect Cercaria
I. Temporal dynamics: Thermal Stress Hypothesis Predictions: Higher levels when current Lower levels following water temperature is high multiple days of warm temperatures
Summer 2015 – Madelyn Messner • Needed a large number of daily cercaria samples from natural sites during peak swimmer’s itch season
Citizen scientists! • Volunteer recruitment & training • Daily samples: July 6 – August 2
Temporal dynamics : July 6 – August 2, 2015 Daily samples- filter Hourly temperature 50L water & light
Sample Processing Collect filter sample Extract DNA qPCR to estimate cercaria abundance
Temporal dynamics: sample processing • 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: statistical analysis Response variable: Log cercaria/ 50L Cercaria/ 50L Min Daily Temp Substantial day to day variation Random effects: - Location - Snail population - Snail infection levels - Bird visitation - Water currents
Temporal dynamics: temporal confoundment EXAMPLE : (Hypothetical) Ocean wind speed • Pirate attacks correlate Pirate attacks with ocean wind speed • Can we conclude increased wind speed caused the increase in pirate attacks through time? 1780 1785 1790 1755 1750 Problem: YEAR • 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)
Temporal dynamics: temporal confoundment 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 *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
Temporal dynamics: Results Random variation…. ( singlicate analyses) Best model according to AIC: 3 predictors Higher cercaria levels in past 5 days → 1. higher cercaria levels today 2. Current temps positive trend 3. Past temps significant negative effect χ 2 Predictor variable Coefficient p-value Log cercaria prev 5 days 23.9 <0.001 1.94 Min daily water temp 0.24 2.66 0.10 Previous 5 day water temp 14.0 <0.001 -0.69
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
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
II. Large-Scale Spatial Survey (16 lakes; 38 sites) What determines patterns of schistosome cercariae abundance across a broad landscape? • >50 volunteers trained Jason • >1040 cercaria samples collected & • >3000 miles driven Ryan • >2500 qPCR assays run Maddie Aleena & Alex & Jenna
What determines SWIMMER’S swimmer’s itch at a ITCH! particular SITE? Cercariae Wind/Waves? in water Snail population Percent snails Cercariae produced density infected per snail Algal Bird Temperature? growth? infection? Possible environmental drivers…..
Hypothesized − Insecticide runoff Arthropod predators drivers: (crayfish) − Land Use Zebra mussels • Urbanization Water clarity • Agriculture Herbicide runoff − • Vegetation − • Development Attached algae Nutrient pollution (N, P) Physical charateristics • Wave action Snail density • Lake size/depth Bird visitation • Substrate type • Temperature Infected snails Temperature Cercariae in water Water clarity hypotheses*: 1. Clear water lets light penetrate to bottom of lake 2. Algal periphyton is often light-limited, especially in deeper water 3. Snail populations are often limited by periphyton (food) abundance 4. Trematode abundance often limited by abundance of host snails
2016 survey parameters (>60 possible predictors….): 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
Results Part 1: Snails responded to water clarity Supported a core prediction of our water clarity hypotheses….
HOWEVER: Snails were dominated by Pleurocera …
Pleurocera drove the Turbidity pattern…
… 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 Encyclopedia of Life: Trichobilharzia sp. parasites Pleurocera collection records
Results 2: Cercariae responded to Stagnicola • No added predictive power by adding other snail species to the analysis
Cercaria levels versus Stagnicola density:
Comparing 2015 & 2016 datasets:
“ Stagnicola ” snails: “ Stagnicola ” snails: Stagnicola catascopium/emarginata/elodes 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…? Encyclopedia of Life: Stagnicola collection records
“ Stagnicola ” snails: Stagnicola catascopium/emarginata/elodes
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?
Results 3: Submerged vegetation reduced cercariae (after accounting for snail density) F 1,35 = 7.0; P = 0.012 Sites with few or no Stagnicola snails How could submerged vegetation reduce the influx of cercariae from other sites?
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