Pteronarcys Californica Research Articles

An unusually large genome from an unusually large stonefly: a chromosome-length genome assembly for the giant salmonfly, Pteronarcys californica (Plecoptera: Pteronarcyidae).

Pteronarcys californica (Newport 1848) is commonly referred to as the giant salmonfly and is the largest species of stonefly (Insecta: Plecoptera) in the western United States. Historically, it was widespread and abundant in western rivers, but populations have experienced a substantial decline in the past few decades, becoming locally extirpated in numerous rivers in Utah, Colorado, and Montana. Although previous research has explored the ecological variables conducive to the survivability of populations of the giant salmonfly, a lack of genomic resources hampers exploration of how genetic variation is spread across extant populations. To accelerate research on this imperiled species, we present a de novo chromosomal-length genome assembly of P. californica generated from PacBio HiFi sequencing and Hi-C chromosome conformation capture. Our assembly includes 14 predicted pseudo chromosomes and 98.8% of Insecta universal core orthologs. At 2.40 gigabases, the P. californica assembly is the largest of available stonefly assemblies, highlighting at least 9.5-fold variation in assembly size across the order. Repetitive elements (REs) account for much of the genome size increase in P. californica relative to other stonefly species, with the content of Class I retroelements alone exceeding the entire assembly size of all but two other species studied. We also observed preliminary suborder-specific trends in genome size that merit testing with more robust taxon sampling.

Thermal tolerance of giant salmonfly nymphs (Pteronarcys californica) varies across populations in a regulated river.

Warming of aquatic ecosystems is transforming the distribution, phenology and growth of the organisms dependent upon these ecosystems. Aquatic insects such as stoneflies are especially vulnerable to warming because the aquatic nymph stage of their life cycle depends on cool, well-oxygenated, flowing water habitat. We tracked thermal effects on available aerobic capacity of the aquatic nymph stage of an iconic and vulnerable stonefly species, the giant salmonfly (Pteronarcys californica), to compare habitat thermal regime measurements for two salmonfly populations from habitats separated by a gradient in summer weekly maximum temperatures. Contrary to expectations, the thermal optima range of the warmer habitat population was cooler than for the cooler habitat population. We posit that this unexpected interpopulation variation in thermal response is more strongly driven by diel and seasonal thermal variability than by the highest summer temperatures experienced within respective habitats. Additionally, we show that summer daily maximum temperatures could result in periodic limits in available aerobic capacity to support work of the warmer habitat nymphs and may be the mechanism underlying reduced abundance relative to the upstream cooler habitat population. Our findings provide insight into potential thermal and metabolic mechanisms that could regulate the success of ecological and culturally important aquatic insect species experiencing global change. We conclude that thermal regimes and thermal variation, not just mean and maximum temperatures, are critical drivers of aquatic insect responses to water temperatures.

Emergence phenology of the giant salmonfly and responses by birds in Idaho river networks

Emergence of adult aquatic insects from rivers is strongly influenced by water temperature, and emergence timing helps to determine the availability of this ephemeral food resource for birds and other terrestrial insectivores. It is poorly understood how spatial heterogeneity in riverine habitat mediates the timing of emergence. Such spatiotemporal variation may have consequences for terrestrial insectivores that rely on aquatic-derived prey resources. We investigated emergence phenology of the giant salmonfly, Pteronarcys californica, at three spatial scales in two Idaho river networks. We examined the influence of tributary confluences on salmonfly emergence timing and associated insectivorous bird responses. Salmonfly emergence timing was highly variable at the basin-scale during the period we sampled (May–June). Within sub-drainage pathways not punctuated by major tributaries, emergence followed a downstream-to-upstream pattern. At the scale of reaches, abrupt changes in thermal regimes created by 10 major tributary confluences created asynchrony in emergence of 1–6 days among the 20 reaches bracketing the confluences. We observed 10 bird species capturing emerged salmonflies, including 5 species typically associated with upland habitats (e.g., American robin, red-tailed hawk, American kestrel) but that likely aggregated along rivers to take advantage of emerging salmonflies. Some birds (e.g., Lewis’s woodpecker, western tanager, American dipper) captured large numbers of salmonflies, and some of these fed salmonflies to nestlings. Emergence asynchrony created by tributaries was associated with shifts in bird abundance and richness which both nearly doubled, on average, during salmonfly emergence. Thermal heterogeneity in river networks created asynchrony in aquatic insect phenology which prolonged the availability of this pulsed prey resource for insectivorous birds during key breeding times. Such interactions between spatial and temporal heterogeneity and organism phenology may be critical to understanding the consequences of fluxes of resources that link water and land. Shifts in phenology or curtailment of life history diversity in organisms like salmonflies may have implications for these organisms, but could also contribute to mismatches or constrain availability of pulsed resources to dependent consumers. These could be unforeseen consequences, for both aquatic and terrestrial organisms, of human-driven alteration and homogenization of riverscapes.

Going with the flow - how a stream insect, Pteronarcys californica, exploits local flows to increase oxygen availability.

For insects, life in water is challenging because oxygen supply is typically low compared with in air. Oxygen limitation may occur when oxygen levels or water flows are low or when warm temperatures stimulate metabolic demand for oxygen. A potential mechanism for mitigating oxygen shortages is behavior - moving to cooler, more oxygenated or faster flowing microhabitats. Whether stream insects can make meaningful choices, however, depends on: (i) how temperature, oxygen and flow vary at microspatial scales and (ii) the ability of insects to sense and exploit that variation. To assess the extent of microspatial variation in conditions, we measured temperature, oxygen saturation and flow velocity within riffles of two streams in Montana, USA. In the lab, we then examined preferences of nymphs of the stonefly Pteronarcys californica to experimental gradients based on field-measured values. Temperature and oxygen level varied only slightly within stream riffles. By contrast, flow velocity was highly heterogeneous, often varying by more than 125 cm s-1 within riffles and 44 cm s-1 around individual cobbles. Exploiting micro-variation in flow may thus be the most reliable option for altering rates of oxygen transport. In support of this prediction, P. californica showed little ability to exploit gradients in temperature and oxygen but readily exploited micro-variation in flow - consistently choosing higher flows when conditions were warm or hypoxic. These behaviors may help stream insects mitigate low-oxygen stress from climate change and other anthropogenic disturbances.

Exposure to copper increases hypoxia sensitivity and decreases upper thermal tolerance of giant salmonfly nymphs (Pteronarcys californica)

Many aquatic insects are exposed to the dual stressors of heavy metal pollution and rising water temperatures from global warming. These stresses may interact and have stronger impacts on aquatic organisms if heavy metals interfere with the ability of these organisms to handle high temperatures. Here we focus on the effect of copper on upper thermal limits of giant salmonfly nymphs (Order: Plecoptera, Pteronarcys californica), a stonefly species which is common in parts of western North America. Experimental exposure to copper reduced upper thermal limits by ∼ 10 °C in some cases and depressed the hypoxia tolerance (Pcrit) of nymphs by ∼ 0.5 mg L−1 DO. These results suggest that copper inhibits the delivery of oxygen, which may explain, in part, the strong reductions in CTMAX that we report. Fluorescence microscopy of Cu-exposed individuals indicated high levels of copper in chloride cells but no clear evidence of damage to or high levels of copper on the gills themselves. Our study indicates that populations of aquatic insects from copper-polluted environments may be further at risk to future warming than those from uncontaminated environments.

Plasticity of salmonfly (Pteronarcys californica) respiratory phenotypes in response to changes in temperature and oxygen.

Like all taxa, populations of aquatic insects may respond to climate change by evolving new physiologies or behaviors, shifting their range, exhibiting physiological and behavioral plasticity, or going extinct. We evaluated the importance of plasticity by measuring changes in growth, survival and respiratory phenotypes of salmonfly nymphs (the stonefly Pteronarcys californica) in response to experimental combinations of dissolved oxygen and temperature. Overall, smaller individuals grew more rapidly during the 6-week experimental period, and oxygen and temperature interacted to affect growth in complex ways. Survival was lower for the warm treatment, although only four mortalities occurred (91.6% versus 100%). Nymphs acclimated to warmer temperatures did not have higher critical thermal maxima (CTmax), but those acclimated to hypoxia had CTmax values (in normoxia) that were higher by approximately 1°C. These results suggest possible adaptive plasticity of systems for taking up or delivering oxygen. We examined these possibilities by measuring the oxygen sensitivity of metabolic rates and the morphologies of tracheal gill tufts located ventrally on thoracic segments. Mass-specific metabolic rates of individuals acclimated to warmer temperatures were higher in acute hypoxia but lower in normoxia, regardless of their recent history of oxygen exposure during acclimation. The morphology of gill filaments, however, changed in ways that appeared to depress rates of oxygen delivery in functional hypoxia. Our combined results from multiple performance metrics indicate that rising temperatures and hypoxia may interact to magnify the risks to aquatic insects, but that physiological plasticity in respiratory phenotypes may offset some of these risks.

Exposure to Copper Increases Hypoxia Sensitivity and Decreases Upper Thermal Tolerance Limits of Giant Salmonfly Nymphs (Pteronarcys Californica)

Exposure to Copper Increases Hypoxia Sensitivity and Decreases Upper Thermal Tolerance Limits of Giant Salmonfly Nymphs (Pteronarcys Californica)

Dietary composition and fatty acid content of giant salmonflies ( Pteronarcys californica ) in two Rocky Mountain rivers

AbstractMany aquatic invertebrates are declining or facing extinction from stressors that compromise physiology, resource consumption, reproduction, and phenology. However, the influence of these common stressors specifically on consumer–resource interactions for aquatic invertebrate consumers is only beginning to be understood. We conducted a field study to investigate Pteronarcys californica (i.e., the “giant salmonfly”), a large‐bodied insect that is ecologically and culturally significant to rivers throughout the western United States. We sampled gut contents and polyunsaturated fatty acid composition of salmonflies to compare resource consumption across river (Madison or Gallatin, Montana), sex (male or female), and habitat (rock or woody debris). We found that allochthonous detritus comprised the majority of salmonfly diets in the Gallatin and Madison Rivers, making up 68% of the gut contents on average, followed by amorphous detritus, diatoms, and filamentous algae. Diets showed little variation across river, sex, or length. Minor differences in diets were detected by habitat type, with a higher proportion of diatoms in the diets of salmonflies collected from rocky habitat compared to woody debris. Fatty acid composition generally supported the results of gut content analysis but highlighted the importance of primary producers. The presence of eicosapentaenoic acid (20:5n‐3) and alpha linolenic acid (18:3n‐3) indicated consumption of diatoms and filamentous green algae, respectively. Our research underscores the importance of a healthy riparian zone that provides allochthonous detritus for invertebrate nutrition as well as the role of algae as an important source of fatty acids.

Flow increases tolerance of heat and hypoxia of an aquatic insect.

Recent experiments support the idea that upper thermal limits of aquatic insects arise, at least in part, from a lack of sufficient oxygen: rising temperatures typically stimulate metabolic demand for oxygen more than they increase rates of oxygen supply from the environment. Consequently, factors influencing oxygen supply, like water flow, should also affect thermal and hypoxia tolerance. We tested this hypothesis by measuring the effects of experimentally manipulated flows on the heat and hypoxia tolerance of aquatic nymphs of the giant salmonfly (Plecoptera: Pteronarcys californica), a common stonefly in western North America. As predicted, stoneflies in flowing water (10 cm s-1) tolerated water that was approximately 4°C warmer and that contained approximately 15% less oxygen than did those in standing water. Our results imply that the impacts of climate change on streamflow, such as changes in patterns of precipitation and decreased snowpack, will magnify the threats to aquatic insects from warmer water temperatures and lower oxygen levels.

Estimating densities of larval Salmonflies (Pteronarcys californica) through multiple pass removal of post-emergent exuvia in Colorado rivers.

Traditional methods of collecting, sorting, and identifying benthic macroinvertebrate samples are useful for stream biomonitoring and ecological studies, however, these methods are time consuming, expensive, and require taxonomic expertise. Estimating larval densities through collection of post-emergent exuvia can be a practical and time efficient alternative. We evaluated the use of multiple pass depletion techniques of the post-emergent exuvia of Pteronarcys californica to estimate larval densities at ten sites in three Colorado rivers. Exuvia density was highly correlated with both final-instar larval density (R2 = 0.90) and total larval density (R2 = 0.88) and the multiple pass removal technique performed well. Exuvia surveys found P. californica at three low density sites where benthic sampling failed to detect it. At moderate and high density sites the exuvia surveys always produced lower density estimates than benthic surveys. Multiple pass depletion estimates of exuvia proved to be an accurate and efficient technique at estimating larval densities and provided an effective alternative for traditional benthic sampling when objectives are detecting and monitoring P. californica, especially at low density sites.

Thermal variability drives synchronicity of an aquatic insect resource pulse

AbstractSpatial heterogeneity in environmental conditions can prolong food availability by desynchronizing the timing of ephemeral, high‐magnitude resource pulses. Spatial patterns of water temperature are highly variable among rivers as determined by both natural and anthropogenic features, but the influence of this variability on freshwater resource pulse phenology is poorly documented. We quantified water temperature and emergence phenology of an aquatic insect (salmonfly, Pteronarcys californica) resource pulse in two rivers characterized by differing catchment topography and human impact. Along both rivers, salmonfly emergence occurred earlier where spring temperatures were warmer. Emergence events were brief (4–8 d) at sites in the more human‐impacted river, but occurred asynchronously along the entire river, lasting 27 d in total. In contrast, emergence events were more prolonged (6–11 d) at sites on the more natural and topographically complex river, but occurred synchronously along the entire river, lasting 13 d in total. These scale‐specific differences in subsidy duration could have opposing consequences for salmonfly consumers depending on their mobility and foraging habits. Asynchronous emergence at a large scale is potentially most important for mobile consumers like birds and fish that can migrate to feed on aquatic insects and track resource waves across a landscape, whereas prolonged emergence duration at a smaller scale may be most important for immobile or opportunistic consumers like spiders and ants. Relating environmental heterogeneity and resource pulse phenology across a gradient of human impact and at multiple spatial scales is needed for a better understanding of how food availability, aquatic–terrestrial linkages, and consumer–resource dynamics may change with climate variability and increasing human activity in the future.

Water temperature drives variability in salmonfly abundance, emergence timing, and body size

AbstractFreshwater organisms are disproportionately impacted by climate change and human disturbance, resulting in shifts in species' distributions and life histories. We coupled contemporary and historical datasets documenting physical and ecological variables over four decades to quantify changes in the abundance, emergence timing, and body size of salmonflies (Pteronarcys californica) in the Madison River in southwest Montana. In contemporary surveys, water temperature was the main driver of salmonfly abundance, emergence timing, and body size. Salmonfly densities were negatively correlated with summer water temperature, which explained 60% of variation in larval density among sites, whereas substrate type played a negligible role. Emergence occurred 20 days earlier, and male and female exuvia length were 13.8% and 11.3% shorter, respectively, at the warmest site relative to the coolest site (4°C difference). These patterns were supported by historical data. For example, a 1.2°C increase in mean annual water temperature in the Madison River between 1977 and 2017 coincided with evidence for upstream range contraction. Between 1973 and 2017, emergence timing varied widely among years, occurring up to 41 days earlier in years when spring water temperatures were relatively warm. As climate change progresses, we predict that salmonflies could be extirpated from an additional 28 km of currently occupied habitat, representing a 22.6% reduction in suitable habitat along the Madison River. This study provides evidence of long‐term biological change of an aquatic insect and highlights the importance of combining spatial and historical datasets to better understand species' responses to environmental stressors across both space and time.

Pulsed salmonfly emergence and its potential contribution to terrestrial detrital pools

Adult aquatic insects are a globally important subsidy in terrestrial food webs. However, our understanding of their importance is largely limited to studies that measure predation of live insects by terrestrial predators. Yet the flux of adult aquatic insects to terrestrial detrital pools may also be an important subsidy pathway, particularly in cases where insect production exceeds the consumption capacity of predators. We used empirical measures of giant salmonfly (Pteronarcys californica) emergence from 37 sites to model potential detrital deposition in nearshore riparian soil food webs. Typically, giant salmonflies emerge en masse for one week each year, and can be locally superabundant. Median detrital deposition by salmonflies ranged between 0.4 and 0.7 gC, 0.04 to 0.09 gN, and 0.002 to 0.005 gP/m2/yr, depending on whether 25% or 100% of available salmonflies entered detrital pools. For a small number of sites with large salmonfly populations, deposition equaled or exceeded annual secondary production of terrestrial insects, annual atmospheric N deposition, and annual atmospheric P deposition. The fact that these values rival yearly nutrient budgets is particularly striking because giant salmonfly deposition represents a subsidy from a single species emerging over a single week. The consequences of this deposition in terrestrial food webs are largely unknown, but it is likely that salmonflies can have important effects on nearshore soil nutrient budgets similar in magnitude to those of other important ecosystem processes.

Phylogeographic comparison of five large-bodied aquatic insect species across the western USA

Glacial legacy, barriers to migration, and dispersal abilities are important determinants of intraspecific genetic diversity. Genetic comparisons can elucidate the distribution of genetic variants among populations, but for many groups of organisms the concordance of population genetic structure and historical refugia among co-occurring species remains unclear. We compared phylogeographic histories of 4 stoneflies (Calineuria californica, Hesperoperla pacifica, Pteronarcys californica, and Pteronarcys princeps) and 1 caddisfly (Dicosmoecus gilvipes) across their species ranges. Study species had large body and wing sizes that suggest strong flying ability and dispersal potential. Nevertheless, riverine habitat restrictions and mating behaviors can inhibit dispersal. We used mitochondrial and nuclear gene sequences to examine population genetic structure relative to potential past and present barriers to dispersal in the western USA. North–south population genetic structure was present for each species but was more pronounced for 2 stoneflies (C. californica and P. californica) and the caddisfly. For these 3 species, phylogenies indicated concordant clades north and south of San Francisco Bay, a large, saltwater estuary in California. Basal phylogenetic nodes and regional centers of haplotype diversity suggested common historical refugia in northern California or southern Oregon, similar to that found in previous studies of salamanders. For 1 stonefly (C. californica) and the caddisfly, distinct populations in the Sierra Nevada Mountains suggested potential barriers to gene flow. The presence of population genetic structure suggests vulnerability to loss of intraspecific diversity under climate change scenarios, particularly for populations at high elevations.

Loss of Genetic Diversity and Increased Subdivision in an Endemic Alpine Stonefly Threatened by Climate Change.

Much remains unknown about the genetic status and population connectivity of high-elevation and high-latitude freshwater invertebrates, which often persist near snow and ice masses that are disappearing due to climate change. Here we report on the conservation genetics of the meltwater stonefly Lednia tumana (Ricker) of Montana, USA, a cold-water obligate species. We sequenced 1530 bp of mtDNA from 116 L. tumana individuals representing “historic” (>10 yr old) and 2010 populations. The dominant haplotype was common in both time periods, while the second-most-common haplotype was found only in historic samples, having been lost in the interim. The 2010 populations also showed reduced gene and nucleotide diversity and increased genetic isolation. We found lower genetic diversity in L. tumana compared to two other North American stonefly species, Amphinemura linda (Ricker) and Pteronarcys californica Newport. Our results imply small effective sizes, increased fragmentation, limited gene flow, and loss of genetic variation among contemporary L. tumana populations, which can lead to reduced adaptive capacity and increased extinction risk. This study reinforces concerns that ongoing glacier loss threatens the persistence of L. tumana, and provides baseline data and analysis of how future environmental change could impact populations of similar organisms.

Note on Mortality of the Emerging StoneflyPteronarcys californicaon the Jocko River, Montana, USA

ABSTRACT. Cold air temperatures may have killed several emerging nymphs and adult Pteronarcys californica on the Jocko River, Montana. Some aquatic insect taxa emerge early on the Jocko River, likely due to warm water temperatures in winter and spring. At this location, P. californica emerges approximately 5–7 weeks earlier than it does on many other streams or rivers across the United States. We hypothesize that this earlier emergence may be a mortality factor when cold fronts cause air temperatures to drop below freezing. Other mortality factors are also discussed.

Genetic evidence for cohort splitting in the merovoltine stonefly Pteronarcys californica (Newport) in Blacksmith Fork, Utah

The life cycles of many stream insects results in the simultaneous existence of multiple cohorts within populations. If larval development is fixed in these long-lived species, successive cohorts may be reproductively isolated and genetically distinct. We examined levels of genetic differentiation in a 333 bp region of the mitochondrial cytochrome-b gene among cohorts of the stonefly Pteronarcys californica (Newport) (Plecoptera, Pteronarcyidae) at two sites along Blacksmith Fork, Utah. Body measurements were collected from 224 specimens. The frequency distribution of (head width) X (head + thorax length) suggests four (Low site) and five year (High site) life cycles comprising an ∼one year embryonic diapause followed by either three or four years of larval development. Seventy-seven individuals were sequenced, from which we detected five unique mtDNA haplotypes. The overall AMOVA suggested moderate genetic differentiation among cohorts (F ST = 0.11, p = 0.01; ΦST = 0.11, p = 0.007). However, pairwise analyses indicated that a single cohort drove the overall ΦST value. Thus, we conclude that there is considerable gene flow among most cohorts of P. californica in Blacksmith Fork.

Phylogeographic and nested clade analysis of the stonefly Pteronarcys californica (Plecoptera:Pteronarcyidae) in the western USA

AbstractLong-distance dispersal by aquatic insects can be difficult to detect because direct measurement methods are expensive and inefficient. When dispersal results in gene flow, signs of that dispersal can be detected in the pattern of genetic variation within and between populations. Four hundred seventy-five base pairs of the mitochondrial gene, cytochrome b, were examined to investigate the pattern of genetic variation in populations of the stonefly Pteronarcys californica and to determine if long-distance dispersal could have contributed to this pattern. Sequences were obtained from 235 individuals from 31 different populations in the western United States. Sequences also were obtained for Pteronarcella badia, Pteronarcys dorsata, Pteronarcys princeps, Pteronarcys proteus, and Pteronarcys biloba. Phylogenies were constructed using all of the samples. Nested clade analysis on the P. californica sequence data was used to infer the processes that have generated the observed patterns of genetic variati...

Numerical and per capita responses to species loss: mechanisms maintaining ecosystem function in a community of stream insect detritivores

We experimentally reduced the diversity of detritivorous stream insects in field enclosures, and measured the effects on an ecosystem function, processing of leaf litter. Two dominant species were removed separately, the stonefly Pteronarcys californica and the caddisfly Lepidostoma unicolor. In principle, processing could be maintained after species loss in two ways: the remaining species could increase their rates of shredding (per capita response), or they could increase in abundance (numerical response). We imposed a numerical response in some treatments by experimentally increasing abundances of either all the remaining species or the other dominant species so that expected metabolic capacity of the assemblage returned to full‐diversity levels. Numerical responses were generally effective in maintaining leaf breakdown when either Lepidostoma or Pteronarcys was removed, except that the treatment in which Lepidostoma was replaced by an equivalent metabolic capacity of all remaining species showed less leaf loss than the full‐diversity treatment. Per capita responses by other species appeared effective in compensating for the removal of Pteronarcys (although there were other explanations) but were not effective in compensating for the removal of Lepidostoma. In summary, the consequences of reduced biodiversity varied with which species was lost and how the remainder responded. Thus there was no simple relationship between biodiversity and ecosystem functioning. However, when numerical or per capita compensation does occur, stability of function should rise with diversity in such “interactive” assemblages.

Effect of springtime water temperature on the time of emergence and size of Pteronarcys californica in the Henry's Fork catchment, Idaho, U.S.A.

1. The emergence time of Pteronarcys californica in streams in the Henry's Fork catchment, Idaho, U.S.A. was negatively correlated with mean April water temperature. Emergence was in mid‐ to late May at sites influenced by groundwater, where April water temperature averaged 7.9 °C. Adults emerged in mid‐June in streams receiving run‐off from snowmelt (mean April water temperature 5.4 °C). Intermediate emergence times were observed in a regulated section of river where water temperature was influenced, on one bank, by dam release (mean April water temperature 4.5 °C) and, on the other, by a spring‐fed tributary stream (mean April water temperature 6.3 °C). 2. During each of the three study years, emergence was earlier on the bank of the regulated section that was warmer during April and May. The mean body length of P. californica exuviae, collected from the warm side of the river, averaged 1.2 mm longer than those collected from the cold side. 3. We tested the effect on emergence of altering springtime water temperature by translocating P. californica in cages from one location to another during April. Individuals moved to sites with higher April water temperature emerged earlier than individuals that remained at the site from which they were collected.