RABO Workshop – RABO Larval Ecology

The goal of being a tadpole is to graze and avoid predators to reach metamorphosis

Algae and temperature explain…

…why frogs don’t breed in the tributaries where they spend the rest of the year

Periphyton and temperature affects development rate

Warmer temperatures improve growth and size at metamorphosis…

up to a certain point

Cyanobacteria and parasites under very warm low flow conditions

Thermal preference
range matches peak
performance range

Impacts of Parasites

Avoiding warm temperatures is adaptive

Smaller metamorph body size

Possible association with limb abnormalities

Bullfrogs have relatively higher prevalence and tolerance of parasites

Superior competitors to R. boylii

Temperature
effects on size
influence
predation risk

Reciprocal transplant experiments

Temperature
effects on size
influence
predation risk

Reciprocal transplant experiments

Predators have a bigger impact
at lower temperatures

Same results with late stage
tadpoles and dragonfly nymphs

Dams change food quality for tadpoles

Collected periphyton covered cobbles in three rivers.

Raised tadpoles in growth chambers and replicated the diurnal temperature fluctuation of the warm peaking and cold peaking rivers.

Dams change thermal regime

Hypolimnetic releases of cold water

Relationship between population size & temperature mirrors larval thermal performance

Summary

R. boylii tads are terrific grazers and thermoregulators

Many factors influence performance

Type of periphyton
Presence of competitors
Presence of predators
Flow velocity

Populations are robust where conditions for tadpoles are optimal

Drought-Disease
Connection

Hana Moidu, Stephanie Carlson, Pablo Rodriguez-Lozano, UC Berkeley
Robert Leidy, EPA
Alessandro Catenazzi, FIU
Marcia Grefsrud, CDFW
Steven Bobzien, EBRPD
Andrea Adams, UCSB

Ecohydrology (https://doi.org/10.1002/eco.2395)

R. boylii susceptible to chytridiomycosis

Museum and Field Surveys

Padgett-Flohr & Hopkins (2009, 2010)
- Bd+ in SF Bay Area since 1966
Lowe (2009)
- Bd+ juvs = reduced body condition
Adams et al. (2017)
- Bd mortality at Alameda Ck.
- Multiple predictors of infection
  - bullfrog presence
  - breeding density
  - streamflow

Range-wide geographic patterns in historical and contemporary fungal infections in the threatened Foothill Yellow-legged Frog, Rana boylii

Belasen, A. M., Peek, R. A., Adams, A. J., Russell, I. D., De León, M. E., Adams, M. J., Bettaso, J, Breedveld, K. G. H., Catenazzi, A., Dillingham, C.P., Grear, D. A., Halstead, B., Johnson, P., Kleeman, P. M., Koo, M.S., Koppl, C.W., Lauder, J. D., Padgett-Flohr, G., Piovia-Scott, J., Pope, K. L., Vredenburg, V., Westphal, M., Wiseman, K., and Kupferberg, S. J.

Affiliations:

Department of Integrative Biology, University of Texas at Austin, Austin, TX, USA.
Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, USA.
Center for Watershed Sciences, UC Davis, Davis, CA, USA.
Earth Research Institute, University of California, Santa Barbara, CA, USA.
Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, Santa Barbara, CA, USA.
Genome Center, University of California, Davis, Davis, CA, USA.
U.S. Geological Survey, Forest and Rangeland Ecosystem Science Center, Corvallis, OR 973303.
Spring Rivers Ecological Sciences LLC, Cassel, CA, 96016, USA
Department of Biological Sciences, Florida International University, Miami, FL 33199.
USDA Forest Service, Plumas National Forest, Quincy, CA.
U.S. Geological Survey, Western Ecological Research Center, Dixon Field Station, Dixon, CA 95620.
National Park Service, Pinnacles National Park, Paicines, CA, USA. Museum of Vertebrate Zoology, University of California, Berkeley, CA, USA.
Sierra Streams Institute, Nevada City, CA 95959, USA.
HELIX Environmental Planning, Inc. Roseville, CA
School of Biological Sciences, Washington State University, Vancouver, WA, USA.
USDA Forest Service, Pacific Southwest Research Station, Arcata, CA, USA.
Department of Biology, San Francisco State University, San Francisco, CA, USA 94132
Department of Herpetology, California Academy of Sciences, San Francisco, CA, USA
Dept. of Integrative Biology, University of California, Berkeley, CA, USA

Distribution of sampling sites across California and Oregon, USA over 124 years. A) Locations where Foothill Yellow-legged Frogs, Rana boylii, were sampled for infection by the fungal pathogen Batrachochytrium dendrobatidis (Bd) and assayed by PCR or histology. Museum samples are shown by diamonds and field samples by circles. Filled symbols (museum in gold, field in green) indicate Bd positive samples. Symbols may represent many samples at a single collection locality; see inset bar plots for sample sizes in all samples (top) and Bd-positive samples (bottom). R. boylii clades are circled: South Coast (gray), Central Coast (orange), North Coast (teal), Southern Sierra (green), Northern Sierra (yellow), Feather (navy blue). California Endangered Species Act (CESA) status is listed for each clade in legend as follows: EN = endangered, TH = threatened, SSC = species of special concern. B) South-to-north trend in spread of Bd (positive = filled, negative = open symbols) among museum (1897-2005, diamonds) and field samples (2005-2021, circles). Size of symbols denotes sample size at the HUC-12 (sub-watershed) level. GAM of latitude ~ capture year in positive samples is shown with black curved line and overlaid R2 value (0.133).

Intermittent streams like Coyote and Alameda Ck comprise 66% of CA’s river networks

Persistent
pools are
a haven for
native fauna

Longest lasting
pools harbor
non-native
bullfrogs

Tradeoff:

Dessication vs. Disease

During wet winters bullfrogs move from upland cattle ponds and then when that is followed by a low precipitation year, their tadpoles can successfully over-winter in the absence of disturbance, and complete their life cycle, so in 2018 Stephanie Carlson and her group who had been monitoring the fish populations for several year started catching bullfrog tadpoles in the longest lasting pools. This sets up a tradeoff for the native amphibians, if they breed in the most persistently wet places they face the negative effects of bullfrogs –, if they breed elsewhere they risk having their tadpoles not reach metamorphosis before the channel dewaters.

In addition to being predators and competitors, bullfrogs are also tolerant hosts of Bd. For example, otherwise healthy looking tadpoles can be so infected with chytrid fungus that the keratin on their mouthparts (tooth rows and beak) is de-pigmented.

Methods

Wade/walk channel
Count clutches
Collect swab samples
Map wet vs dry

Chytrid Results

Conclusions

R. boylii is susceptible to Bd in a multiple stressor environment

prevalence
- Sex / stage (males)
- Bullfrogs (reservoir & vector)
- Water year
load
- Mean daily stream flow
  - Dilution effect
- Bullfrogs
- Season
- Con-specific density

In summary, R. boylii does appear to be susceptible to Bd infection in the field when multiple stressors act together. Our mixed effects models showed that bullfrogs are a strong predictor of both Bd prevalence and Bd load. In addition, sexstage, particularly being a male, is a significant predictor of whether a R. boylii individual will be infected. This photo shows a potential reason why males are more likely to be infected, males wrestle each other and congregate at the lek sites; male R. boylii mistake bullfrogs for large female boylii, this is a picture of a boylii in amplexus with a bullfrog. With direct contact with a known Bd reservoir like this, it is easy to imagine how males would be more infected. Also, there was a significant effect of water year on infection. Interestingly, even though the outbreak happened in the early water year of 2014, Bd prevalence was actually much higher in 2015, and the male effect didn’t seem to matter as much. We know that bullfrogs are usually asymptomatic carriers and can provide Bd a reservoir; they can also spread bd to new regions as they disperse. We think that it is what is happening at the little Yosemite site since the year of the outbreak was the first year that bullfrogs were observed that far upstream. Alternatively, stress induced on native species by competition or direct predation by bullfrogs may be suppress the immune system of R. boylii and they become infected. When R. boylii become infected, the intensity of that infection is best predicted by stream flow, bullfrogs, season, and con-specific density. Decreasing bd loads with increasing streamflow is consistent with the hypothesis that a large volume of water dilutes the potential infective zoospore pool, and frogs can disperse throughout lotic environments in the watershed. As flows decrease, ephemeral reaches go dry and pools shrink, we would expect increased density-dependent transmission rates. The take home message is that until now, not much was known about the effects of Bd on this species. Now we know that it is susceptible…

Tadpoles in
agal based food webs

The goal of being a tadpole is to graze and avoid predators to reach metamorphosis

Algae and temperature explain…

Periphyton and temperature affects development rate

Warmer temperatures improve growth and size at metamorphosis…

Cyanobacteria and parasites under very warm low flow conditions

Thermal preference
range matches peak
performance range

Impacts of Parasites

Bullfrogs have relatively higher prevalence and tolerance of parasites

Temperature
effects on size
influence
predation risk

Temperature
effects on size
influence
predation risk

Predators have a bigger impact
at lower temperatures

Same results with late stage
tadpoles and dragonfly nymphs

Dams change food quality for tadpoles

Dams change thermal regime

Relationship between population size & temperature mirrors larval thermal performance

Summary

Drought-Disease
Connection

R. boylii susceptible to chytridiomycosis

Range-wide geographic patterns in historical and contemporary fungal infections in the threatened Foothill Yellow-legged Frog, Rana boylii

Intermittent streams like Coyote and Alameda Ck comprise 66% of CA’s river networks

Persistent
pools are
a haven for
native fauna

Longest lasting
pools harbor
non-native
bullfrogs

Methods

Chytrid Results

Conclusions

Summary of Drought & Disease Effects

Questions?

Tadpoles in agal based food webs

The goal of being a tadpole is to graze and avoid predators to reach metamorphosis

Algae and temperature explain…

Periphyton and temperature affects development rate

Warmer temperatures improve growth and size at metamorphosis…

Cyanobacteria and parasites under very warm low flow conditions

Thermal preference range matches peak performance range

Impacts of Parasites

Bullfrogs have relatively higher prevalence and tolerance of parasites

Temperature effects on size influence predation risk

Temperature effects on size influence predation risk

Predators have a bigger impact at lower temperatures

Same results with late stage tadpoles and dragonfly nymphs

Dams change food quality for tadpoles

Dams change thermal regime

Relationship between population size & temperature mirrors larval thermal performance

Summary

Drought-Disease Connection

R. boylii susceptible to chytridiomycosis

Range-wide geographic patterns in historical and contemporary fungal infections in the threatened Foothill Yellow-legged Frog, Rana boylii

Intermittent streams like Coyote and Alameda Ck comprise 66% of CA’s river networks

Persistent pools are a haven for native fauna

Longest lasting pools harbor non-native bullfrogs

Methods

Chytrid Results

Conclusions

Summary of Drought & Disease Effects

Questions?

Tadpoles in
agal based food webs

Thermal preference
range matches peak
performance range

Temperature
effects on size
influence
predation risk

Temperature
effects on size
influence
predation risk

Predators have a bigger impact
at lower temperatures

Same results with late stage
tadpoles and dragonfly nymphs

Drought-Disease
Connection

Persistent
pools are
a haven for
native fauna

Longest lasting
pools harbor
non-native
bullfrogs