Taricha Torosa Research Articles

Native amphibian toxin reduces invasive crayfish feeding with potential benefits to stream biodiversity

BackgroundBiodiversity is generally reduced when non-native species invade an ecosystem. Invasive crayfish, Procambarus clarkii, populate California freshwater streams, and in the Santa Monica Mountains (Los Angeles, USA), their introduction has led to trophic cascades due to omnivorous feeding behavior and a rapid rate of population growth. The native California newt, Taricha torosa, possesses a neurotoxin, tetrodotoxin (TTX), that affects freshwater animal behavior. Given P. clarkii has a limited evolutionary history with TTX, we hypothesized that TTX may affect crayfish feeding behaviors. To determine if TTX affects P. clarkii behavior, we measured cumulative movement and various feeding behaviors of P. clarkii exposed to (i) waterborne, ecologically realistic concentrations of TTX (~ 3.0 × 10− 8 moles/L), (ii) an anuran chemical cue to account for intraguild cues, or (iii) a T. torosa chemical cue with quantitated TTX in it (~ 6.2 × 10− 8 moles/L).ResultsWe found that the presence of TTX in any form significantly reduced crayfish movement and decreased the amount of food consumed over time. Crayfish responses to the anuran treatment did not significantly differ from controls.ConclusionOur laboratory results show that naturally occurring neurotoxin from native California newts limits invasive crayfish foraging and feeding rates, which may play a role in preserving local stream ecosystems by limiting invasive crayfish behaviors that are detrimental to biodiversity.

The effect of road-based mortality on a local population of newts along a narrow two-lane road in California

Numerous studies have documented high numbers of amphibians killed by vehicular strikes on roads. This direct mortality can cause population declines and extirpations, but in some cases the declines might be masked, initially, by large population sizes. Population viability analysis can help discern population trajectories and identify incipient declines. We applied this tool to a situation in Santa Clara County, California where a dead-on-the-road carcass survey in 2017 demonstrated that a large number of newts in the genus Taricha were being killed by vehicles using a small two-lane road (Alma Bridge Road) most likely during annual breeding migrations to a local reservoir (Lexington Reservoir). To help determine the effect of this road-based mortality on the California newt (T. torosa) population, we conducted a drift fence/pitfall trap array study on the road during the 2020–2021 breeding season. Drift fence/pitfall trap arrays were installed at six locations along a 6.6-km stretch of the road and daily surveys were conducted at these arrays over a 148-day period from mid-November to end of March. Daily traffic and precipitation data were also recorded to help inform timing of proposed mitigation efforts. Concurrently, a group of community scientists conducted a dead-on-the-road carcass survey over the entire 6.6-km study area. We calculated the number of adult newts attempting to cross Alma Bridge Road at the arrays and the associated road-based mortality rates. Then, we combined our array results with road mortality data provided by the community scientists to estimate the number of adult California newts attempting to cross the road and their mortality rates over the entire study area during the survey period. We then incorporated this data into a population viability model to determine whether this road-based mortality rate might, if left unabated, lead to a reduction in, and possibly the eventual extirpation of, the local population of T. torosa breeding in Lexington Reservoir. The model indicated that this population would be extirpated in approximately 92 years. Because the road has been in use for approximately 67 years, we discussed the possible reasons why this population is currently extant and experiencing this high level of road-based mortality.

On the estimation of body mass in temnospondyls: a case study using the large‐bodied Eryops and Paracyclotosaurus

AbstractTemnospondyli are a morphologically varied and ecologically diverse clade of tetrapods that survived for over 200 million years. The body mass of temnospondyls is a key variable in inferring their ecological, physiological and biomechanical attributes. However, estimating the body mass of these extinct creatures has proven difficult because the group has no extant descendants. Here we apply a wide range of body mass estimation techniques developed for tetrapods to the iconic temnospondyls Paracyclotosaurus davidi and Eryops megacephalus. These same methods are also applied to a collection of extant organisms that serve as ecological and morphological analogues. These include the giant salamanders Andrias japonicus and Andrias davidianus, the tiger salamander Ambystoma tigrinum, the California newt Taricha torosa and the saltwater crocodile, Crocodylus porosus. We find that several methods can provide accurate mass estimations across this range of living taxa, suggesting their suitability for estimating the body masses of temnospondyls. Based on this, we estimate the mass of Paracyclotosaurus to have been between 159 and 365 kg, and that of Eryops between 102 and 222 kg. These findings provide a basis for examining body size evolution in this clade across their entire temporal span.

Trophic Relationships in Larval California Newts (Taricha torosa)

The larval stage of the California newt (Taricha torosa) has been little studied despite the presence and abundance of the species throughout much of California. During the 2017–2018 time period, the diet and life history characteristics of this cohort of stream-dwelling newt larvae were examined, using gut contents and stable isotopes, in order to better understand the ecological niche and trophic relationships of the life stage. Our results suggest that the newt larvae consume Chironomidae as a major part of their diet and that this reliance decreases as the larvae age. Newt larvae also feed more widely and abundantly as they age. The isotopic data suggest that as larvae get larger, they alter their diet but that the relationships to both carbon source (δC) and trophic level (δN) are complex.

Resilience of native amphibian communities following catastrophic drought: Evidence from a decade of regional-scale monitoring

The increasing frequency and severity of drought may exacerbate ongoing global amphibian declines. However, interactions between drought and coincident stressors, coupled with high interannual variability in amphibian abundances, can mask the extent and underlying mechanisms of drought impacts. We synthesized a decade (2009–2019) of regional-scale amphibian monitoring data (2273 surveys, 233 ponds, and seven species) from across California's Bay Area and used dynamic occupancy modeling to estimate trends and drivers of species occupancy. An extreme drought during the study period resulted in substantial habitat loss, with 51% of ponds drying in the worst year of drought, compared to <20% in pre-drought years. Nearly every species exhibited reduced breeding activity during the drought, with the occupancy of some species (American bullfrogs and California newts) declining by >25%. Invasive fishes and bullfrogs were also associated with reduced amphibian occupancy, and these taxa were locally extirpated from numerous sites during drought, without subsequent recovery– suggesting that drought may present an opportunity to remove invaders. Despite a historic, multi-year drought, native amphibians rebounded quickly to pre-drought occupancy levels, demonstrating evidence of resilience. Permanent waterbodies supported higher persistence of native species during drought years than did temporary waterbodies, and we therefore highlight the value of hydroperiod diversity in promoting amphibian stability.

Life History Variation in Two Populations of California Newt, Taricha torosa

California Newts (Taricha torosa) are common amphibians throughout much of California, yet their life history has been little studied. We examined T. torosa in 2 physically separated breeding locations, a farm pond and a nearby stream, between February and June 2015. We synoptically collected physical measurements on adults as well as tissue samples from a subset of the newts present in both locations throughout the time period. Stable isotopes of carbon and nitrogen were used to characterize the trophic niche space among newts of different locations and ages. Our results suggest differentiated breeding phenologies as well as unique trophic signatures in the 2 different locations. In our sampling, the pond group bred and developed a few weeks earlier in the season and ate at a higher trophic level, while the stream group bred and developed later and ate lower on the food chain. Taken as a whole, our results suggest that the newts in this area exhibit some degree of ecological and life history plasticity.

The geographic mosaic in parallel: Matching patterns of newt tetrodotoxin levels and snake resistance in multiple predator-prey pairs.

The Geographic Mosaic Theory of Coevolution predicts that coevolutionary arms races will vary over time and space because of the diverse ecological settings and population histories of interacting species across the landscape. Thus, understanding coevolution may require investigating broad sets of populations sampled across the range of the interaction. In addition, comparing coevolutionary dynamics between similar systems may reveal the importance of specific factors that structure coevolution. Here, we examine geographic patterns of prey traits and predator traits in the relatively unstudied interaction between the Sierra garter snake (Thamnophis couchii) and sympatric prey, the rough-skinned newt (Taricha granulosa), Sierra newt (Ta. sierrae) and California newt (Ta. torosa). This system parallels, in space and phenotypes, a classic example of coevolution between predatory common garter snakes (Th. sirtalis) and their toxic newt prey exhibiting hotspots of newt tetrodotoxin (TTX) levels and matching snake TTX resistance. We quantified prey and predator traits from hundreds of individuals across their distributions, and functional trait matching at sympatric sites. We show strong regional patterns of trait covariation across the shared ranges of Th. couchii and newt prey. Traits differ significantly among localities, with lower newt TTX levels and snake TTX resistance at the northern latitudes, and higher TTX levels and snake resistance at southern latitudes. Newts and snakes in northern populations show the highest degree of functional trait matching despite possessing the least extreme traits. Conversely, newts and snakes in southern populations show the greatest mismatch despite possessing exaggerated traits, with some snakes so resistant to TTX they would be unaffected by any sympatric newt. Nevertheless, individual variation was substantial, and appears to offer the opportunity for continued reciprocal selection in most populations. Overall, the three species of newts appear to be engaged in a TTX-mediated arms race with Th. couchii. These patterns are congruent with those seen between newts and Th. sirtalis, including the same latitudinal gradient in trait covariation, and the potential 'escape' from the arms race by snake predators. Such concordance in broad scale patterns across two distinct systems suggests common phenomena might structure geographic mosaics in similar ways.

Tracking the assembly of nested parasite communities: Using β-diversity to understand variation in parasite richness and composition over time and scale.

Community composition is driven by a few key assembly processes: ecological selection, drift and dispersal. Nested parasite communities represent a powerful study system for understanding the relative importance of these processes and their relationship with biological scale. Quantifying β-diversity across scales and over time additionally offers mechanistic insights into the ecological processes shaping the distributions of parasites and therefore infectious disease. To examine factors driving parasite community composition, we quantified the parasite communities of 959 amphibian hosts representing two species (the Pacific chorus frog, Pseudacris regilla and the California newt, Taricha torosa) sampled over 3months from 10 ponds in California. Using additive partitioning, we estimated how much of regional parasite richness (γ-diversity) was composed of within-host parasite richness (α-diversity) and turnover (β-diversity) at three biological scales: across host individuals, across species and across habitat patches (ponds). We also examined how β-diversity varied across time at each biological scale. Differences among ponds comprised the majority (40%) of regional parasite diversity, followed by differences among host species (23%) and among host individuals (12%). Host species supported parasite communities that were less similar than expected by null models, consistent with ecological selection, although these differences lessened through time, likely due to high dispersal rates of infectious stages. Host individuals within the same population supported more similar parasite communities than expected, suggesting that host heterogeneity did not strongly impact parasite community composition and that dispersal was high at the individual host-level. Despite the small population sizes of within-host parasite communities, drift appeared to play a minimal role in structuring community composition. Dispersal and ecological selection appear to jointly drive parasite community assembly, particularly at larger biological scales. The dispersal ability of aquatic parasites with complex life cycles differs strongly across scales, meaning that parasite communities may predictably converge at small scales where dispersal is high, but may be more stochastic and unpredictable at larger scales. Insights into assembly mechanisms within multi-host, multi-parasite systems provide opportunities for understanding how to mitigate the spread of infectious diseases within human and wildlife hosts.

Amphibian responses in the aftermath of extreme climate events

Climate change-induced extinctions are estimated to eliminate one in six known species by the end of the century. One major factor that will contribute to these extinctions is extreme climatic events. Here, we show the ecological impacts of recent record warm air temperatures and simultaneous peak drought conditions in California. From 2008–2016, the southern populations of a wide-ranging endemic amphibian (the California newt, Taricha torosa) showed a 20% reduction to mean body condition and significant losses to variation in body condition linked with extreme climate deviations. However, body condition in northern populations remained relatively unaffected during this period. Range-wide population estimates of change to body condition under future climate change scenarios within the next 50 years suggest that northern populations will mirror the loss of body condition recently observed in southern populations. This change is predicated on latter 21st century climate deviations that resemble recent conditions in Southern California. Thus, the ecological consequences of climate change have already occurred across the warmer, drier regions of Southern California, and our results suggest that predicted climate vulnerable regions in the more mesic northern range likely will not provide climate refuge for numerous amphibian communities.

Resistance and tolerance: A hierarchical framework to compare individual versus family-level host contributions in an experimental amphibian-trematode system

Hosts have two general strategies for mitigating the fitness costs of parasite exposure and infection: resistance and tolerance. The resistance-tolerance framework has been well developed in plant systems, but only recently has it been applied to animal-parasite interactions. However, difficulties associated with estimating fitness, controlling parasite exposure, and quantifying parasite burden have limited application of this framework to animal systems. Here, we used an experimental approach to quantify the relative influence of variation among host individuals and genetic families in determining resistance and tolerance within an amphibian-trematode system. Importantly, we used multiple, alternative metrics to assess each strategy, and employed a Bayesian analytical framework to compare among responses while incorporating uncertainty. Relative to unexposed hosts, exposure to the pathogenic trematode (Ribeiroia ondatrae) reduced the survival and growth of California newts (Taricha torosa) (survival: 93% vs. 74%; growth: 0.29 vs. −0.5 vs mm day −1). Similarly, parasite infection success (the inverse of resistance) ranged from 8% to 100%. Yet despite this broad variation in host resistance and tolerance among individual newts, we found no evidence for transmissable, among-family variation in any of the resistance or tolerance metrics. This suggests that opportunities for evolution of these traits is limited, likely requiring significant increases in mutation, gene flow, or environmental heterogeneity. Our study provides a quantitative framework for evaluating the importance of alternative metrics of resistance and tolerance across multiple time points in the study of host-parasite interactions in animal systems.

Human traffic and habitat complexity are strong predictors for the distribution of a declining amphibian.

Invasive species and habitat modification threaten California's native pond-breeding amphibians, including the federally threatened California Red-legged Frog (Rana draytonii). The relative contributions of invasive species, including the American Bullfrog (Lithobates catesbeianus), and of habitat changes to these declines are disputed. I conducted a field study over several years in central California to examine the presence/absence of these two species at 79 breeding ponds to determine the predictive role for occupancy of factors including vegetation, pond characteristics, and measures of human activity. I used a boosted regression tree approach to determine the relative value of each predictor variable. Increased measures of human activity, especially proximity to trails and roads, were the best predictors for the absence of California Red-legged Frogs and California Newts. Historical factors and habitat conditions were associated with the extent and spread of the American Bullfrog. The extent and complexity of aquatic macrophytes and pond surface area were good predictors for the presence of these and other amphibian species. Surprisingly, invasive species played a relatively small role in predicting pond occupancy by the native species. These findings can inform conservation and restoration efforts for California Red-legged Frogs, which apparently persist best in small vegetated ponds in areas of low human disturbance.

The effect of newt toxin on an invasive snail

Invasive species are well documented to impact native species where they are introduced. In the Santa Monica Mountains, a native species of amphibian, the California newt (Taricha torosa) possesses a neurotoxin, tetrodotoxin (TTX) that is considered a chemical defense against predation but also appears to facilitate ecological processes and specifically affect freshwater macroinvertebrate behavior. A recently introduced invasive species, the New Zealand mud snail (Potamopyrgus antipodarum), is known to negatively affect ecosystems it invades and means to control its proliferation once introduced are limited. Given the ecological role of newt neurotoxin, we hypothesized that TTX may impact P. antipodarum behavior and tested its effects upon snail movement in laboratory assays and in-stream experiments. When snails were exposed to ecologically realistic TTX concentrations and newt chemical cues that contain TTX they moved significantly less and distance was significantly reduced relative to controls. In a natural stream, significantly more P. antipodarum moved out of areas exposed to newt chemical cues relative to snails in the presence of native tree frog cues (Pseudacris cadaverina). Our results suggest that California newts may help limit the spread of P. antipodarum in streams where T. torosa is both able to persist and possess adequate chemical defenses.

An amphibian chemical defense phenotype is inducible across life history stages

Inducible phenotypic responses to environmental variation are ubiquitous across the tree of life, but it remains an open question whether amphibian chemical defense phenotypes are inducible. Tetrodotoxin (TTX) is a key chemical defense trait in North American and Eurasian newts (Salamandridae). We tested if TTX can be induced by exposing populations of adult and larval California newts (Taricha torosa) to sustained stressful conditions while longitudinally quantifying TTX concentrations. Adult newts rapidly increased chemical defenses in response to simulated predator attacks and consistently maintained elevated TTX concentrations relative to wild, non-captive individuals. We also found that laboratory-reared larvae maintained chemical defenses nearly three-fold greater than those of siblings reared in streams. Collectively, our results indicate that amphibian chemical defenses are not fixed. Instead, toxins are maintained at a baseline concentration that can quickly be increased in response to perceived risk with substantial increases to toxicity. Therefore, it is crucial that inducible variation be accounted for when considering ecological dynamics of chemically defended animals and coevolutionary predator-prey and mimic-model relationships.

Marine Biotoxins: Occurrence, Toxicity, and Detection Methods

This review summarizes the role of marine organisms as vectors of marine biotoxins, and discusses the need for surveillance to protect public health and ensure the quality of seafood. I Paralytic shellfish poison (PSP) and PSP-bearing organisms-PSP is produced by toxic dinoflagellates species belonging to the genera Alexandrium, Gymnodinium, and Pyrodinium. Traditionally, PSP monitoring programs have only considered filter-feeding molluscs that concentrate these toxic algae, however, increasing attention is now being paid to higher-order predators that carry PSP, such as carnivorous gastropods and crustaceans. II. Tetrodotoxin (TTX) and TTX-bearing organisms - TTX is the most common natural marine toxin that causes food poisonings in Japan, and poses a serious public health risk. TTX was long believed to be present only in pufferfish. However, TTX was detected in the eggs of California newt Taricha torosa in 1964, and since then it has been detected in a wide variety of species belonging to several different phyla. In this study, the main toxic components in the highly toxic ribbon worm Cephalothrix simula and the greater blue-ringed octopus Hapalochlaena lunulata from Japan were purified and analysed.

Predicting the effects of manual crayfish removal on California newt persistence in Santa Monica Mountain streams

We construct a hybrid, stage-structured mathematical model to study whether trapping of the invasive predatory crayfish Procambarus clarkii can prevent local extinctions of the California newt (Taricha torosa), a species of special concern native to Santa Monica Mountain streams. Specifically, we numerically and analytically determine under what conditions trapping can drive the crayfish population size to zero. We observe the persistence or the time to extinction for newt populations under corresponding trapping scenarios. No simulations allow for long-term coexistence of newts and crayfish, although multiple scenarios delay newt extinction by several years in the presence of crayfish. We predict that crayfish extinction and newt persistence become more likely as the quantity of trapping resources, frequency of trapping implementation, and susceptibility of the crayfish population to trapping increases. We quantify the effectiveness of different crayfish trapping regimes at delaying the time until the newt population goes extinct. Predictions made with our model inform restorative efforts and crayfish management.

Responses of a wetland ecosystem to the controlled introduction of invasive fish

Summary The ecological consequences of species invasions can vary in time and space, complicating efforts to generalise invader impacts across ecosystems. This challenge is particularly relevant when using small‐scale experiments to derive predictions for freshwater ecosystems. In this study, our aims were to document the effects of a controlled fish introduction within an ecosystem‐scale experiment and to test possible factors driving variation in invasion outcomes. We measured community and ecosystem responses to the introduction of western mosquitofish (Gambusia affinis: Poeciliidae) using a ‘Before‐After‐Control‐Impact’ design within a large, experimentally divided natural wetland in California, USA. We then used a replicated outdoor mesocosm experiment to address how two factors that vary widely in natural wetlands – habitat complexity and alternative prey availability – mediate the effects of mosquitofish on native wetland amphibians. In the natural wetland, mosquitofish increased in population size by ˜90‐fold over the course of a single summer. Mosquitofish introduction was associated with a 50% decrease in macroinvertebrate density and a 90% decrease in zooplankton abundance relative to a fishless control treatment. We observed no effects of mosquitofish on the abundance or total biomass of two native pond‐breeding amphibians – the Pacific chorus frog (Pseudacris regilla: Hylidae) and California newt (Taricha torosa: Salamandridae) – likely because more preferable alternative prey were abundant, vegetation provided refuges from predation, and the mosquitofish introduction occurred after amphibian larval stages were most susceptible to predation. Surprisingly, mosquitofish were also associated with a 50% decrease in both relative phytoplankton fluorescence and total phosphorus, and a sharp increase in N:P ratios in the water column, possibly due to the assimilation of fish biomass acting as a nutrient sink. In contrast to our ecosystem experiment, mosquitofish consumed native amphibians and reduced their growth rates in outdoor mesocosms. The strength of predation within the smaller scale venue, however, varied with the availability of alternative prey (i.e. zooplankton), and the complexity of the habitat (i.e. presence of aquatic macrophytes). Our mesocosm results support the hypothesis that alternative prey and habitat complexity facilitated coexistence between invasive mosquitofish and native amphibian larvae in our ecosystem experiment. Our findings highlight the potential for invasive fish to drive rapid shifts in freshwater ecosystems while also emphasising the roles of environmental characteristics in mediating whether native and non‐native species will coexist.

A discrete stage-structured model of California newt population dynamics during a period of drought

We introduce a mathematical model for studying the population dynamics under drought of the California newt (Taricha torosa), a species of special concern in the state of California. Since 2012, California has experienced a record-setting drought, and multiple studies predict drought conditions currently underway will persist and even increase in severity. Recent declines and local extinctions of California newt populations in Santa Monica Mountain streams motivate our study of the impact of drought on newt population sizes. Although newts are terrestrial salamanders, they migrate to streams each spring to breed and lay eggs. Since egg and larval stages occur in water, a precipitation deficit due to drought conditions reduces the space for newt egg-laying and the necessary habitat for larval development. To mathematically forecast newt population dynamics, we develop a nonlinear system of discrete equations that includes demographic parameters such as survival rates for newt life stages and egg production, which depend on habitat availability and rainfall. We estimate these demographic parameters using 15 years of stream survey data collected from Cold Creek in Los Angeles County, California, and our model captures the observed decline of the parameterized Cold Creek newt population. Based upon data analysis, we predict how the number of available newt egg-laying sites varies with annual precipitation. Our model allows us to make predictions about how the length and severity of drought can affect the likelihood of persistence and the time to critical endangerment of a local newt population. We predict that sustained severe drought will critically endanger the newt population but that the newt population can rebound if a drought is sufficiently short.

Individual fluctuations in toxin levels affect breeding site fidelity in a chemically defended amphibian.

Behaviours that influence habitat selection strongly determine species movement patterns. One component of animal behaviour that largely influences movement patterns and habitat choice is site fidelity. California newts (family Salamandridae) demonstrate remarkable site fidelity, typically homing to the same pool of a stream each breeding season. Individuals often occupy a specific pool throughout the breeding season, but some males shift among breeding pools, altering their set of potential mates, competitors, and predators. In this study, we measured dermal concentrations of the chemical defence compound tetrodotoxin (TTX) in recaptured male California newts (Taricha torosa) over five breeding seasons to evaluate whether relative TTX concentrations are associated with breeding site fidelity in the field. Our five years of field sampling indicates that TTX concentrations of individuals and group means fluctuate tremendously, implying that TTX is not a stable phenotypic trait. Despite such fluctuations, we found that an individual's relative TTX concentration explains fidelity to a breeding pool and suggests that newts may be able to assess both their own concentrations of TTX and that of conspecifics to make decisions about remaining in or abandoning a breeding pool. These results provide us a novel dimension to chemical defence phenotypes in nature and their ecological consequences, potentially requiring a re-evaluation of the coevolutionary dynamics of predation pressure on toxin-laden organisms.

Corrigendum to “Quantifying tetrodotoxin levels in the California newt using a non-destructive sampling method” [TOXCON 80 (2014) 87-93

Corrigendum to “Quantifying tetrodotoxin levels in the California newt using a non-destructive sampling method” [TOXCON 80 (2014) 87-93

Removal Efforts and Ecosystem Effects of Invasive Red Swamp Crayfish (Procambarus clarkii) in Topanga Creek, California

Red swamp crayfish (Procambarus clarkii) were first recorded in Topanga Creek in 2001. When the onset of drought in Southern California resulted in low flows and warming water temperatures from 2011–2014, the population rapidly increased. Within the Santa Monica Mountains, P. clarkii has been linked to diminishing numbers of California newt (Taricha torosa), a species of special concern (Kats et al. 2013). To address these concerns, a student-based citizen science program was conducted from November 2013 through April 2014 to remove crayfish from a 200 m reach of Topanga Creek. The following data was collected and compared between the removal reach and an upstream, adjacent 200 meter non-removal reach (control): water quality (temperature, salinity, pH, conductivity, dissolved oxygen, turbidity), nutrient levels (nitrate, nitrite, ammonia, orthophosphate), benthic macroinvertebrate community metrics, crayfish demographics and catch-per unit effort (removal reach only). The results indicate that red swamp crayfish presence or removals do not affect water quality or nutrient levels in Topanga Creek. However, benthic macroinvertebrate communities were significantly different between reaches; the presence of crayfish correlated with lower BMI abundance and species richness, higher proportion of tolerant taxa, and lower feeding group complexity.