skip to main content


Title: Threshold elemental ratios and the temperature dependence of herbivory in fishes
Abstract

Herbivorous ectothermic vertebrates are more diverse and abundant at lower latitudes. While thermal constraints may drive this pattern, its underlying cause remains unclear. We hypothesized that this constraint stems from an inability to meet the elevated phosphorus demands of bony vertebrates feeding on P‐poor plant material at cooler temperatures because low gross growth efficiency at warmer temperatures facilitates higher P ingestion rates. We predicted that dietary carbon:phosphorus (C:P) should exceed the threshold elemental ratio between carbon and P‐limited growth (TERC:P) for herbivores feeding at cooler temperatures, thereby limiting the range of herbivorous ectothermic vertebrates facing P‐limited growth.

We tested this hypothesis using the Andean suckermouth catfishesAstroblepusandChaetostoma.Astroblepusare invertivores that inhabit relatively cool, high‐elevation streams whileChaetostomaare grazers that inhabit relatively warm, low‐elevation streams. We calculated TERC:Pfor each genus across its elevational range and compared these values to measured values of food quality over an elevational gradient in the Andes. We also broadly summarized measurements of TERC:Pacross diverse groups of fishes.

Supporting our hypothesis, we found that dietary C:P was predicted to exceed the TERC:Pfor the grazerChaetostomanear the highest elevation where this genus has been recorded. Conversely, the TERC:Pfor the invertivoreAstroblepuswas consistently higher than that ofChaetostomaand thus its dietary C:P never approached the TERC:P. We found that, among all fishes, omnivores had higher average TERC:Pthan invertivores, and TERC:Pdid not vary with temperature.

Our results suggest that, at least for Andean suckermouth catfishes, cool temperatures constrain herbivory at higher elevations. Increased gross growth efficiency at cooler temperatures evidently restricts the ability of P‐limited consumers to meet P demand. However, our survey of fish TERC:Pestimates suggests that some fishes are able to circumvent this constraint through behavioural and life‐history adaptations that reduce P demand or increase P use efficiency.

The physiological trade‐offs underlying these functional shifts reveal that geographic dietary patterns can be predicted by stoichiometric theory, but variation in food quality and consumer traits that reduce P demand and/or increase P efficiency can create exceptions to these patterns.

Aplain language summaryis available for this article.

 
more » « less
NSF-PAR ID:
10461379
Author(s) / Creator(s):
 ;  ;  ;  ;
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Functional Ecology
Volume:
33
Issue:
5
ISSN:
0269-8463
Page Range / eLocation ID:
p. 913-923
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Ecologically relevant symbioses are widespread in terrestrial arthropods but based on recent findings these specialized interactions are likely to be especially vulnerable to climate warming. Importantly, empirical data and climate models indicate that warming is occurring asynchronously, with night‐time temperatures increasing faster than daytime temperatures. Daytime (DTW) and night‐time warming (NTW) may impact ectothermic animals and their interactions differently as DTW results in greater daily temperature variation and moves organisms nearer to their thermal limits, while NTW avoids thermal limits and may relieve constraints of cooler night‐time temperatures; a nuance that has largely been ignored in the literature.

    In laboratory experiments, we investigated how the timing of warming influences a widespread defensive mutualism involving the pea aphidAcyrthosiphon pisum, and its heritable symbiont,Hamiltonella defensa, which protects against an important natural enemy, the parasitic waspAphidius ervi.

    Three aphid sublines were experimentally created from single aphid genotype susceptible toA. ervi: one line infected with a highly protectiveH. defensastrain, one infected with a moderately protective strain and one without any facultative symbiont. We examined aphid fitness in the presence and absence of parasitoids and when exposed to an average 2.5°C increase occurring across three warming scenarios (night‐time vs. daytime vs. uniform) relative to no‐warming controls.

    An increase of 2.5°C, as predicted to occur by the IPCC before 2100, was sufficient to disable the aphid defensive mutualism regardless of the timing of warming; a surprising result given that the daily maxima for control and NTW scenarios were identical. We also found that warming negatively impacted (a) symbiont‐mediated interactions between host and parasitoid more than symbiont‐free ones; (b) species interactions (host–parasitoid) more than each participant independently and (c) aphids more than parasitoids even though higher trophic levels are generally predicted to be more affected by warming.

    Here we show that 2.5°C warming, regardless of timing, negatively impacted a common microbe‐mediated defensive mutualism. While this was a laboratory‐based study, results suggest that temperature increases predicted in the near‐term may disrupt the many ecological symbioses present in terrestrial ecosystems.

     
    more » « less
  2. Abstract

    Lakes are vulnerable to climate change, and warming rates in the Arctic are faster than anywhere on Earth. Fishes are sensitive to changing temperatures, which directly control physiological processes. Food availability should partly dictate responses to climate change because energetic demands change with temperature, but few studies have simultaneously examined temperature and food availability.

    We used a fully factorial experiment to test effects of food availability and temperature (7.6, 12.7, and 17.4°C; 50 days) on growth, consumption, respiration, and excretion, and effects of temperature (12 and 19.3°C; 27 days) on habitat use and growth of a common, but understudied, mid‐level consumer, slimy sculpinCottus cognatus, in arctic lakes. We also used bioenergetics modelling to predict consumptive demand under future warming scenarios.

    Growth rates were 3.4× higher at 12.7°C in high food compared to low food treatments, but the magnitude of differences depended on temperature. Within low food treatments, there was no statistical difference in growth rates among temperatures, suggesting food limitation. Consumption, respiration, and nitrogen excretion increased with temperature independent of food availability. Lower growth rates coincided with lower phosphorus excretion at the highest temperature, suggesting that fish selectively retained phosphorus at high temperatures and low food. In habitat choice experiments, fish were more likely to use the 12°C side of the tank, closely matching their optimal temperature. We predicted a 9% increase in consumption is required to maintain observed growth under a 4°C warming scenario.

    These results highlight considering changes in food resources and other associated indirect effects (e.g. excretion) that accompany changing temperatures with climate change. Depending on how food webs respond to warming, fish may cope with predicted warming if density‐dependent feedback maintains population sizes.

     
    more » « less
  3. Abstract

    The abiotic environment drives species abundances and distributions both directly and indirectly through effects on multi‐trophic species interactions. However, few studies have documented the individual and combined consequences of these direct and indirect effects.

    We studied an ant‐tended aphid along an elevational gradient, where lower elevations were more arid. Hypotheses of stronger species interactions at lower elevations and a greater sensitivity of higher trophic levels to climate led us to predict increased top‐down control of aphids by natural enemies (third trophic level) but even stronger protection from mutualist ants (fourth trophic level) with increasing aridity. As a result, we predicted that mutualism strength and aphid abundance would increase with aridity.

    We documented patterns of aphid abundance and tested for both the direct and multi‐trophic indirect effects of aridity on aphid performance. To do so, we used both observational and manipulative methods across two years in replicate high‐ and low‐elevation valleys, where summer temperatures decreased by 3.7°C and precipitation increased by 27 mm/mo from low to high elevations.

    Aphid colonies were 75% larger in the most (vs. least) arid sites, and this was best explained by changes in interactions with predators and ants. Aphids were unaffected by the direct effects of the abiotic environment or its indirect effects via host plant quality. In contrast, natural enemy effects increased with aridity; under ant exclusion, natural enemies had no effect on aphids in the least arid sites but depressed colony growth by 252% in the most arid sites. Ant activity also increased with aridity, with ants discovering more aphid colonies and experimental baits and allocating more foragers per aphid, although there was no effect of aridity on ant abundance or community composition. Correspondingly, the mutualist services provided by ants increased with aridity; ants provided no benefits to aphids in the least arid sites but doubled colony growth in the most arid sites.

    In summary, an elevational cline in herbivore abundance was driven by a monotonic increase in trophic‐level sensitivity to aridity. These findings illustrate that predicting species responses to climate change will require a multi‐trophic perspective.

     
    more » « less
  4. Abstract

    A possible response of many plant species to global warming is migration to higher elevations. However, these migrations may not be required if species can tolerate higher temperatures, or may be prevented if there are other factors such as changes in soil conditions that make upslope areas unsuitable.

    We used a set of 3‐year field transplant experiments in the remote Peruvian Andes to simulate two possible responses of an abundant tropical montane cloudforest tree species (Weinmania bangii) to global warming: (a) ‘upward migration’, in which case seedlings ofW. bangii'swere grown at their current elevation/temperature but in soils transplanted from higher elevations and (b) ‘migration failure’, in which case seedlings were transplanted downslope along with their home soils into areas that are 1°C or 2°C warmer. We conducted separate experiments with populations from the upper/leading edge, middle and lower/trailing edges ofW. bangii'selevational/thermal range to assess the influence of local adaptation on responses to changes in temperature or soil.

    We found that seedling survival and growth were not affected by changes in soil conditions, regardless of the origin population. However, seedling survival decreased with temperature. A simulated warming of 1°C caused a significant reduction in the survival of seedlings transplanted from the mid‐range population, and 2°C warming caused a severe decrease in the survival of seedlings transplanted from both the mid‐range and bottom‐edge populations.

    Synthesis. Our findings reveal that rising temperatures are a serious threat to plants, especially in populations growing in the hotter portion of their species’ range. At least in the case ofW. bangii,novel soil conditions will not limit the establishment or growth of seedlings at higher elevations. As such, decreases in the survivorship at lower elevations may be offset through upward migrations as temperatures continue to increase.

     
    more » « less
  5. Abstract

    The coordination of traits from individual organs to whole plants is under strong selection because of environmental constraints on resource acquisition and use. However, the tight coordination of traits may provide underlying mechanisms of how locally adapted plant populations can become maladapted because of climate change.

    To better understand local adaptation in intraspecific trait coordination, we studied trait variability in the widely distributed foundation tree species,Populus fremontiiusing a common garden near the mid‐elevational point of this species distribution. We examined 28 traits encompassing four spectra: phenology, leaf economic spectrum (LES), whole‐tree architecture (Corner's Rule) and wood economic spectrum (WES).

    Based on adaptive syndrome theory, we hypothesized that trait expression would be coordinated among and within trait spectra, reflecting local adaptation to either exposure to freeze‐thaw conditions in genotypes sourced from high‐elevation populations or exposure to extreme thermal stress in genotypes sourced from low‐elevation populations.

    High‐elevation genotypes expressed traits within the phenology and WES that limit frost exposure and tissue damage. Specifically, genotypes sourced from high elevations had later mean budburst, earlier mean budset, higher wood densities, higher bark fractions and smaller xylem vessels than their low‐elevation counterparts. Conversely, genotypes sourced from low elevations expressed traits within the LES that prioritized hydraulic efficiency and canopy thermal regulation to cope with extreme heat exposure, including 40% smaller leaf areas, 67% higher stomatal densities and 34% higher mean theoretical maximum stomatal conductance. Low‐elevation genotypes also expressed a lower stomatal control over leaf water potentials that subsequently dropped to pressures that could induce hydraulic failure.

    Synthesis. Our results suggest thatPopulus fremontiiexpresses a high degree of coordination across multiple trait spectra to adapt to local climate constraints on photosynthetic gas exchange, growth and survival. These results, therefore, increase our mechanistic understanding of local adaptation and the potential effects of climate change that in turn, improves our capacity to identify genotypes that are best suited for future restoration efforts.

     
    more » « less