We lack a strong understanding of how organisms with complex life histories respond to climate variation. Many stream-associated species have multi-stage life histories that are likely to influence the demographic consequences of floods and droughts. However, tracking stage specific demographic responses requires high-resolution, long-term data that are rare. We used eight years of capture-recapture data for the headwater stream salamander Gyrinophilus porphyriticus to quantify the effects of flooding and drying magnitude on stage-specific vital rates and population growth. Drying reduced larval recruitment but increased the probability of metamorphosis (i.e., adult recruitment). Flooding reduced adult recruitment but had no effect on larval recruitment. Larval and adult survival declined with flooding but were unaffected by drying. Annual population growth rates (lambda, ) declined with flooding and drying. Lambda also declined over the study period (2012 – 2021), although mean was 1.0 over this period. Our results indicate that G. porphyriticus populations are resilient to hydrologic variation due to compensatory effects on recruitment of larvae vs. adults (i.e., reproduction vs. metamorphosis). Complex life cycles may enable this resilience to climate variation by creating opportunities for compensatory demographic responses across stages. However, more frequent and intense hydrologic variation in the latter half of this study contributed to a decline in over time, suggesting that increasing environmental variability poses a threat even when demographic compensation occurs.
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Hydrologic variability contributes to reduced survival through metamorphosis in a stream salamander
Changes in the amount, intensity, and timing of precipitation are increasing hydrologic variability in many regions, but we have little understanding of how these changes are affecting freshwater species. Stream-breeding amphibians—a diverse group in North America—may be particularly sensitive to hydrologic variability during aquatic larval and metamorphic stages. Here, we tested the prediction that hydrologic variability in streams decreases survival through metamorphosis in the salamander Gyrinophilus porphyriticus , reducing recruitment to the adult stage. Using a 20-y dataset from Merrill Brook, a stream in northern New Hampshire, we show that abundance of G. porphyriticus adults has declined by ∼50% since 1999, but there has been no trend in larval abundance. We then tested whether hydrologic variability during summers influences survival through metamorphosis, using capture–mark–recapture data from Merrill Brook (1999 to 2004) and from 4 streams in the Hubbard Brook Experimental Forest (2012 to 2014), also in New Hampshire. At both sites, survival through metamorphosis declined with increasing variability of stream discharge. These results suggest that hydrologic variability reduces the demographic resilience and adaptive capacity of G. porphyriticus populations by decreasing recruitment of breeding adults. They also provide insight on how increasing hydrologic variability is affecting freshwater species, and on the broader effects of environmental variability on species with vulnerable metamorphic stages.
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- Award ID(s):
- 1655653
- PAR ID:
- 10130441
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences
- Volume:
- 116
- Issue:
- 39
- ISSN:
- 0027-8424
- Page Range / eLocation ID:
- 19563 to 19570
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Assessing direct fitness effects of individual genetic diversity is challenging due to the intensive and long‐term data needed to quantify survival and reproduction in the wild. But resolving these effects is necessary to determine how inbreeding and outbreeding influence eco‐evolutionary processes. We used 8 years of capture–recapture data and single nucleotide polymorphism genotypes for 1906 individuals to test for effects of individual heterozygosity on stage‐specific survival probabilities in the salamanderGyrinophilus porphyriticus. The life cycle ofG. porphyriticusincludes an aquatic larval stage followed by metamorphosis into a semi‐aquatic adult stage. In our study populations, the larval stage lasts 6–10 years, metamorphosis takes several months, and lifespan can reach 20 years. Previous studies showed that metamorphosis is a sensitive life stage, leading us to predict that fitness effects of individual heterozygosity would occur during metamorphosis. Consistent with this prediction, monthly probability of survival during metamorphosis declined with multi‐locus heterozygosity (MLH), from 0.38 at the lowest MLH (0.10) to 0.06 at the highest MLH (0.38), a reduction of 84%. Body condition of larvae also declined significantly with increasing MLH. These relationships were consistent in the three study streams. With evidence of localised inbreeding within streams, these results suggest that outbreeding disrupts adaptations in pre‐metamorphic and metamorphic individuals to environmental gradients along streams, adding to evidence that headwater streams are hotspots of microgeographic adaptation. Our results also underscore the importance of incorporating life history in analyses of the fitness effects of individual genetic diversity and suggest that metamorphosis and similar discrete life stage transitions may be critical periods of viability selection.more » « less
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{"Abstract":["This data set includes spatially explicit mark-recapture data of the\nNorthern Spring Salamander (Gyrinophilus porphyriticus) collected during\nthe summer months (June \u2013 August) from downstream and upstream reaches\nin multiple streams in the Hubbard Brook Experimental Forest. Downstream\nreaches begin at the confluence with the Main Hubbard and extend\nupstream 500 meters and upstream reaches begin at the weir and extend\ndownstream 500 meters. Downstream reaches contain brook trout and\nupstream reaches do not. We used a robust design framework with\napproximately 9 surveys per reach each summer (3 primary occasions with\n3 secondary occasions each). Salamanders were captured by hand and\nmarked with either Visual Implant Elastomer and/or a PIT tag.\n These data were gathered as part of the Hubbard Brook Ecosystem Study\n(HBES). The HBES is a collaborative effort at the Hubbard Brook\nExperimental Forest, which is operated and maintained by the USDA Forest\nService, Northern Research Station.\n These data have been published in the following papers: \n Lowe WH, Addis\nBR, Smith MR, Davenport JM. The spatial structure of variation in\nsalamander survival, body condition and morphology in a headwater stream\nnetwork. Freshwater Biol. 2018;63:1287\u20131299.\nhttps://doi.org/10.1111/fwb.13133\n Lowe, W. H., and Addis, B. R.. 2019. Matching habitat choice and plasticity contribute to phenotype\u2013environment covariation in a stream salamander. Ecology 100( 5):e02661. 10.1002/ecy.2661 \n Lowe, W.H., et al. Hydrologic variability contributes to reduced survival through metamorphosis in a stream salamander. Proceedings of the National Academy of Sciences 2019; 116.39: 19563-19570.\n Bryant, A.R., Gabor, C.R., Swartz, L.K., Wagner, R., Cochrane, M.M., Lowe, W.H. Differences in corticosterone release rates of larval Spring Salamanders (Gyrinophilus porphyriticus) in response to native fish presence. Biology 2022; 11.484. https://doi.org/10.3390/biology11040484\n Addis, B.R., and W.H. Lowe. Environmentally associated variation in dispersal distance affects inbreeding risk in a stream salamander." The American Naturalist 2022."]}more » « less
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