https://orcid.org/0000-0002-1310-0268
Figures
Abstract
An important impact of global warming in nature is the decline of ecological functions such as primary production, habitat provision, and carbon sequestration. These functions can be disrupted when the species that perform them are impaired by anthropogenic warming or other stressors. Where there is a diversity of responses to warming among the species filling these roles, the function is more likely to be maintained despite the loss of the least tolerant species. However, the response diversity to warming of key functions is generally unknown, particularly for the roles played by predatory and marine species. Here, we show that the thermal sensitivity of predation to acute warming varies substantially among four marine invertebrate carnivores: three whelks and a sea star that inhabit rocky reefs around the Galápagos islands. Two of the four predators were clearly adapted to cooler temperatures and their functional performance declined dramatically with experimental warming. In contrast, predation by two whelks, and one in particular, improved with warming, including beyond temperatures expected in 2100 under the most pessimistic emissions scenario. These results suggest that a high level of temperature response diversity of predation could help maintain this critical function in a variable and changing environment.
Citation: Chico-Ortiz N, Agudo-Adriani E, Capone HE, Silva I, Brandt M, Bruno JF (2025) Predator response diversity to warming enables ecosystem resilience in the Galápagos. PLOS Clim 5(1): e0000652. https://doi.org/10.1371/journal.pclm.0000652
Editor: Jennifer Lee Wilkening, US Fish and Wildlife Service, UNITED STATES OF AMERICA
Received: May 22, 2025; Accepted: December 1, 2025; Published: January 21, 2026
Copyright: © 2026 Chico-Ortiz et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All project data is available at https://github.com/eagudoadriani/PredationDiversity_Warming.
Funding: This study was funded by the National Science Foundation (OCE #2128592 to JFB and MB). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Introduction
The core functions of natural ecosystems — that ultimately provide the services humans depend on — are performed by groups of species with similar characteristics, e.g., pollinators and decomposers [1,2]. Warming and numerous other aspects of climate change impair these species and their ability to perform ecological functions [3–8]. Due to the universality of metabolic scaling between temperature and the metabolism of ectothermic organisms, the rates of many ecosystem functions also scale with temperature [9,10]. This temperature-function relationship is typically unimodal, initially increasing with temperature up to a threshold (known as the thermal optimum), then declining rapidly [10]. The tipping point at which functioning declines is determined by the thermal sensitivity of the species most tolerant of warming.
The diversity of warming responses among the species that make up a functional group (i.e., “ecological response diversity”) is believed to influence the resilience of ecosystem functions to disturbance and environmental change [11–14]. If most or all species within a functional group have similar tolerances of and responses to warming, most of the group and the function itself will be lost if temperature increases (Fig 1). In contrast, a diversity of responses and thermal niches, and in particular the presence of one or more species tolerant of warming, can help maintain functioning even if species richness declines [11,13] (Fig 1).
Each curve represents the functional response of a species (A-F) within a single functional group, e.g., herbivores or detritivores. Left: the functional responses of the three species are very similar, and response diversity is low. Right: functional response diversity is greater, and this community is likely to be more resistant to warming (in this case) or another type of disturbance or environmental change. Note the functional response of these species is often measured as metabolism or fitness. This can be informative, but it is often better to directly measure the species’ actual functional performance based on its specific ecological role, e.g., herbivory.
Response diversity can be, but is not necessarily related to, species richness [11,13]. For example, Tilman and Downing [15] demonstrated that temperate grassland plots with greater species richness were more likely by chance to include drought-tolerant species. Therefore, when a drought occurred, the most diverse experimental plots were the most resistant to reductions in rainfall and were able to maintain ecological functions like primary production and habitat provision. In contrast, even on the world’s most biodiverse coral reefs there is little variation in thermal tolerance among species within functional groups such as the fast-growing and habitat-providing acroporid corals [16]. In the Indo-Pacific, anthropogenic heatwaves only one or two degrees C above typical conditions can kill off dozens of species within this functional group of reef corals [17]. In this case, species richness is a poor predictor of ecosystem resistance to warming, because although functional redundancy is very high [18] (i.e., many species can fill the same functional role), response diversity within this taxonomic and functional group appears to be relatively low.
Moreover, the ability of an organism or species to survive an acute or chronic disturbance is not necessarily indicative of its ongoing functional performance; the per capita performance of a species can be low or even zero even though it is still present in a community. Therefore, ecological response diversity cannot be inferred indirectly by measuring species richness or even the presence of functionally important species and instead must be measured directly. As a result, very little is known about the response diversity of complex ecological functions in nature [13,16,19,20].
There is some prior work in marine systems on response diversity and climate resilience. For example, Nash et al. [21] found that when response diversity of herbivorous fishes that inhabit coral reefs is high, top-down control of seaweeds is maintained even when heat waves reduce the abundance of smaller parrotfishes, apparently benefitting larger-bodied herbivores. Moreover, coral communities at those locations recover more rapidly. Likewise, a modeling study [22] found that response diversity to warming and other disturbances among tropical corals can support ecological resilience. Coral communities comprised of species with high resistance as well as species able to recover rapidly, were more resilient to disturbance. In the model, the two types of corals facilitated recovery by the other through “competitor-enabled rescue”.
We quantified the functional response diversity of marine carnivores to ocean warming. We measured the effects of warming on the metabolism and predation rates of four invertebrate carnivores from rocky subtidal reefs of the Galápagos including three whelks and one sea star (Fig 2). Our results indicate a high degree of functional response diversity among marine carnivores in this system and suggest this characteristic could enable functional resilience to anthropogenic warming.
(A) Heliaster cumingi, (B) Hexaplex princeps, (C) Tribulus planospira, and (D) Vasula melones. The three prey species used were (E) Megabalanus peninsularis, (F) Columbella haemastoma (note this image is of the visually very similar congener C. fuscata), and (G) Engina pirostoma. In the experiments, predator species A-C were fed Megabalanus and Vasula were fed the two small herbivorous snails (F and G). Species sizes, including their relative sizes, are not to scale. Photos A-D, F, and G were taken by Jose Vieira. E was taken by Favio Rivera.
Materials and methods
Predation experiment
To measure the species-specific effect of temperature on feeding, we quantified the predation rates of four invertebrate carnivores: Vasula melones, Tribulus planospira, Hexaplex princeps, and Heliaster cumingi (Fig 2), hereafter referred to by their genus. These species share a similar diet of barnacles and inhabit the same shallow subtidal rocky reefs and occasionally rocky intertidal habitats. Some have also been observed feeding on mollusks. For example, Vasula feeds on herbivorous snails. The four study consumers were selected based on their abundances, similar diets, their co-occurrence in the same habitats, and their perceived ecological roles as important consumers of barnacles, the dominant prey species on many shallow rocky subtidal reefs in the region. Additionally, we were able to obtain permission and research permits from the Galápagos National Park to collect and work with them inside the protected Galápagos Marine Reserve. All four species are relatively abundant, thus we could collect them for the predation experiment and physiological measurements with minimal effects on natural populations and the local community.
All experiments were performed inside laboratory aquaria at the Galapagos Science Center (GSC) on San Cristóbal Island, Galápagos. Vasula, Tribulus, and Heliaster were collected from Bahía Tijeretas on the southwestern coast of San Cristóbal (0° 53’ 17.0“ S, 89° 36’ 25.0” W) at depths of 1-4 m. Hexaplex was collected from La Barcaza (0°40’ 25.5” S, 89° 15’ 55.0” W, Fig A in S1 Text), a small island off the northwestern coast of San Cristóbal at 8 m depth. In the predation experiment, Tribulus, Hexaplex, and Heliaster were fed barnacles (Megabalanus peninsularis) and Vasula were fed small herbivorous snails (Columbella haemastoma and Engina pyrostoma). Vasula were offered different prey because we were unable to collect enough individuals of the large size that regularly eat the barnacle prey. Barnacles were collected at 8 m depth from La Barcaza and intertidally at Kicker Rock (0° 46’ 41.7” S, 89° 31’ 06.9” W). The herbivorous snails used as prey were collected from Tijeretas.
We measured predator feeding rates inside 16 L glass aquaria during May, June, and July of 2021 and 2023. Each aquarium was filled with seawater that was pumped from the nearby ocean, held inside two 2000 L tanks, and filtered using a high-quality filtration system (RainHarvest Systems Triple 20 Inch Big Blue Filter Assembly, Blue, L-R, 20 μm pleated sediment filter, a 5 μm pleated sediment filter, and a 1 μm activated carbon block filter; SKU 17695) to reduce microbial metabolic activity. We replaced one third of the water in each aquarium three times a week and monitored salinity levels twice daily. Throughout the predation experiments, individuals were exposed to 12 h of both light and darkness. Water inside the aquaria was oxygenated using air stones (Marina 1-inch Cylinder Air Stone, model A962) and experimental temperatures were maintained with a thermostat control system (Inkbird ITC-308 Digital Temperature Controller). Once the temperature inside a given aquarium deviated by ± 0.3°C from the desired experimental temperature, the system activated a centralized chiller (AquaEuroUSA Max Chill-1/13 HP Chiller) or an individual submersible heater (Tetra HT30 Submersible Aquarium Heater & Electronic Thermostat, one per aquarium, Fig B in S1 Text). The chiller system was connected to all aquaria and operated independently in each tank via the Inkbird thermostats that controlled the pumps (one per aquarium) which pulled cold water from the chiller through the stainless steel chiller coils in each aquarium. The cold, freshwater pumped through the chiller coils was not mixed with water from other treatments, and the chiller could simultaneously cool several tanks at once, with its activation controlled by each tank’s independent thermostat.
The temperature of the surface and shallow waters of the sea surrounding the Galápagos islands is incredibly dynamic [23]. This is due to the complex interplay of oceanographic phenomena acting at different spatial and temporal scales including the ENSO cycle and seasonal variation in the strength of ocean currents such as the Humbolt current that delivers cold water from the Southern Ocean [23–25]. As a result, ocean surface temperature can be as cool as 12 or 13ºC in the La Niña phase of the ENSO cycle and as warm as 32ºC during El Niño (Fig 3). In addition, the strength of upwelling (the delivery of cool, nutrient rich water from depth) can vary at a scale of tens of meters or minutes, causing variation in seawater temperature of several degrees (ºC) between nearby locations or during a given day [23].
Shaded areas of the graphic indicate the status of the ENSO cycle during the study period (El Niño red, La Niña blue, and neutral conditions in light grey) based on NOAA’s Oceanic Niño Index (ONI) https://www.climate.gov/news-features/understanding-climate/climate-variability-oceanic-nino-index). The four horizontal lines overlaying the temperature data are the estimated mean thermal optima for predation (as shown in Fig 4C) by the four experimental carnivores.
The selection of experimental temperatures was based on field measurements taken at numerous local subtidal sites including Cerro Mundo (Fig 3). The temperatures predators were exposed to covered nearly the full range they experienced on nearby subtidal rocky reefs between 2019 and early 2024 (Fig 3). The lowest temperature we used was 16ºC, which is ~ 1ºC higher than the lowest recorded temperatures (we could not reliably maintain experimental temperatures below 16ºC). Experimental temperatures varied somewhat among predators (Table 1) based on pilot studies indicating that some species could not tolerate higher temperatures. Due to space and other resource limitations in the laboratory, all temperature incubations and experiments across the four predator species were conducted asynchronously.
For the predation experiments with Tribulus, Hexaplex, and Heliaster, barnacle prey were epoxied (Z SPAR Splash Zone 2-Part Epoxy Compound) to small stones and placed in the aquaria (Fig C in S1 Text). Two barnacles were used for Tribulus, while between four and seven barnacles were used for Hexaplex and Heliaster. For the Vasula treatment, five herbivorous snails were added to each aquarium. Predation was monitored daily by checking for the presence of consumed prey, and any consumed prey were replaced within 12 h. The general approach was to ensure that the predators had easy access to prey, with minimal time required for searching. While predator searching is a crucial component of predator-prey interactions that can be influenced by temperature [26], in this experiment we focused on how temperature affected consumption rates when the search for prey was minimal and standardized across temperatures. To assess the effect of temperature on prey mortality, one control aquarium was included for each temperature incubation per predator, where prey were exposed to the same conditions as the experimental trials but without predators. Two control replicates (n = 2) were included for barnacles at 16°C, 26°C and 28°C, as these temperatures were included in all predator experiments. No significant effect of temperature on prey mortality was observed as no prey died in the control aquaria at any temperature.
Respiration measurements
We also measured the species-specific effect of temperature on metabolism measured as respiration in physiology chambers at eleven ecologically relevant temperatures (16, 20, 24, 26, 28, 30, 32, 34, 36, 40, 42°C). The experimental temperatures went well beyond what is observed naturally in the predators’ environment because this is typically required to estimate organismal TPCs and TPC metrics such as Topt (i.e., the function cannot be reliably modeled without temperatures well past Topt). Thermal performance trials were conducted on a single species each day over a two-week period in July 2022 and 2023 at the GSC. Prior to each trial, species were collected from their aforementioned locations and held overnight in seawater at a constant temperature of 16°C, close to the ambient temperature of the seawater in situ. The following day, individuals of a given species (n = 9 for Tribulus and Vasula) were randomly assigned to one of ten acrylic 680-mL respirometry chambers containing filtered seawater (as described above). The tenth chamber was left empty as a control to measure background metabolic activity (e.g., by microbes in the seawater) during thermal trials, and this rate was later subtracted from the rates of all other chambers at the corresponding experimental temperature. For Hexaplex and Heliaster, sample sizes were reduced (n = 5) because they required larger chambers, and the closer spacing of measurement compartments within the closed respirometry system limited the number of individuals that could be run simultaneously. Once sealed, all chambers were placed in slots on a motorized respirometry table (Australian Institute of Marine Science) housed inside a 142 L cooler (Quick and Cool 150 Qt Cooler, Item #: 00044363) filled with seawater at the experimental temperature (Fig D in S1 Text). Magnetic stir bars rotated at ~200 rpm to ensure water circulation, oxygen saturation, and stable, uniform temperatures throughout the trials.
Oxygen consumption was measured using a PreSens Oxygen Meter System (OXY-10 SMA [G2] Regensburg, Germany) with fiber-optic oxygen probes (PreSens dipping probes [DP-PSt7-10-L2.5-ST10-YOP]) and temperature probes (Pt1000) recording respiration rate inside each chamber every 1 s for ~15 min. These measurements were recorded using PreSens Measurement Studio 2 software (v.3.0.3.1703). Temperature was maintained to within ± 0.3°C of the experimental temperature for a given incubation by a thermostat that controlled a heater-chiller system (as previously described). Any measurement abnormalities (e.g., the organism or a bubble touching the oxygen probe causing a false oxygen spike) were noted and later removed from the data prior to analysis.
After each temperature incubation, individuals remained in their chambers (lids unscrewed for oxygen exchange) and were placed in a 120 L container with filtered seawater at the previous incubation temperature for 10–20 min to standardize acclimation. During this time, the cooler housing the respirometry table was warmed to the next temperature, and air stones aerated and circulated the water. Once the seawater had warmed to the next experimental temperature, the ten chambers were replenished and situated in their respective table positions for the following incubation. After the final temperature incubation, water volume displacement was measured for each chamber and used to estimate the amount of water inside the chamber to normalize the oxygen concentration measurements. Individuals were then euthanized by placing them in a labeled ziplock bag overnight in a 5°C freezer. The following day, they were desiccated at 60°C for 24 h in a drying oven (Memmert UFE 400 Sterilizer Laboratory Oven) and incinerated at 500°C for 4 h in a muffle furnace (Optic Ivymen System Laboratory Furnace 8.2/1100). Post-burn weights (g) were subtracted from pre-burn weights to normalize respiration rates by Ash-Free Dry Weight (AFDW).
Thermal performance curves and analysis
The PreSens oxygen consumption measurements collected for each individual during a given temperature incubation were used to derive the metabolic slope for that organism’s temperature incubation. This rate can then be represented as a single point (i.e., of nine total replicates) at each incubation, forming a TPC across the test temperature gradient. To quantify respiration rates obtained from the PreSens system, we used repeated local linear regressions through the LoLinR package in R, which uses a bootstrapping method to determine a rate based on point density (See [27] for further information on model parameters). We performed corrections for chamber water volume displacement (i.e., by each organism) and metabolic rates from control chambers and normalized each rate by its respective individual’s AFDW. These rates were then log-transformed preceding their fit to a modified Sharpe–Schoolfield equation for high-temperature inactivation using a nonlinear least squares regression. Fits were determined using the ‘nls.multsart’ R package [28,29] to generate random starting values for thermal parameters, and we used Akaike Information Criterion (AIC) in model selection for the best-fitting parameter set [28,29]. After obtaining model fits, we used 95% confidence intervals (CIs) to estimate Topt for each species [as in 30]. Once Topt values were obtained, we visually assessed their distribution using histograms and quantile-quantile plots. The interquartile range (IQR) method, substituting the median and IQR for mean and standard deviation (SD) [31,32], was used to identify and remove outliers from each species, as compared to the SD approach, this non-parametric method yields more robust statistics, is less sensitive to small sample sizes, and does not rely on symmetry assumptions.
We constructed a linear model for the Topt values to estimate response diversity among the study species and evaluated model fit using AIC and Bayesian information criterion comparisons. ANOVA assumptions of homogeneity and normality were tested with Levene’s and Shapiro–Wilk’s tests, respectively. We then created bar plots showing the mean (± 1SE) Topt per species and generated four TPCs representing the average metabolic response of each species across the experimental temperature gradient. All data analyses were performed in R v.4.2.2, and the source data and scripts are publicly accessible on GitHub (https://github.com/eagudoadriani/PredationDiversity_Warming).
Results and discussion
We found a high degree of response diversity to acute warming. Our results suggest that despite the potential of functional decline of species intolerant of high temperatures (i.e., with continued ocean warming), other species could fill their role and maintain the ecological function (in this case, predation). Two of our four experimental species (the sea star Heliaster and the whelk Hexaplex) are clearly cold-adapted and highly sensitive to warming. For both, predation was greatest at ~21–22°C (Fig 4C). For example, predation by Hexaplex was low at 16°C (Fig 4C), peaked at 21°C, then declined with temperatures typical of warmer periods and seasons in the Galápagos (i.e., 26°C and 28°C, Fig 3). Heliaster predation (which on a per capita basis was the highest of the four experimental species) was greatest at 22°C and declined to nearly zero at 25°C (Fig 4C).
A) Thermal Performance Curves (TPCs) for each species based on measurements of mass-normalized respiration across a range of temperatures. B) The thermal optima (Topt) of respiration across the four predators, calculated from the TPCs. C) Functional responses of predation to temperature. Vasula were fed two snail prey (Engina pyrostoma and Columbella haemastoma) and the other three predators were fed the barnacle Megabalanus peninsularis. In B and C, solid horizontal lines are mean values and associated vertical shaded bars are ± 1SE, while in A shaded bars are 95% confidence intervals. We fit curves for each species in C using the geom_smooth function in ggplot2 to help visualize the predation TPCs. See Supplementary Information for additional details about the predation experiments and respiration measurements.
At the highest experimental temperature for Heliaster (25°C), several experimental individuals showed signs of stress and died after lesions were observed on their dorsal surface. We have also observed Heliaster with these lesions in the field when ocean temperature exceeds ~24ºC, for example during the 2023–24 El Niño event. The lesions appear similar to the typical signs of sea star wasting disease [33,34]; a common temperature-related disease of sea stars in the U.S. Pacific Northwest. Heliaster cumingi is endemic to the Galápagos and was nearly extirpated during the 1982–1983 El Niño due to extreme high temperatures. Before then it was very common in intertidal and shallow subtidal habitats and was considered an important carnivore in the community. Heliaster has recently recovered in some locations, however, our results suggest that it remains vulnerable to high temperatures and anthropogenic warming.
Two of the whelk species (particularly Vasula) were far more tolerant of higher temperatures. Predation by Tribulus was low at 19°C, peaked around 28°C and declined at 31°C. Vasula did not feed at all at 19°C (Fig 4C) and in contrast to the other three species, its predation continued to increase to the highest experimental temperature for the predation experiment (32°C), indicating an especially high thermal tolerance.
In nature, predation is a complex process that includes interactive behavioral components between predators and prey [35]. Our study was designed to greatly simplify this interaction and focused solely on the narrow act of prey consumption. For example, by providing predators with ample prey (effectively feeding them ad libidum) in a small arena we largely eliminated the need for predators to search for their prey. It is well known that temperature can affect predator search time and prey avoidance behaviors and escape velocity [26,36]. Thus, it is possible our results would have been different had we included these components, although to do so we would have had to perform the experiments in much larger containers with more realistic surfaces. Moreover, prey density can strongly affect predation [35], in large part because it influences predator search time, and it is plausible that changing the number or density of prey in our experiments could have influenced predation rates.
An important caveat is that one of the four predators (Vasula) was fed snails instead of barnacles. Although large Vasula commonly consume barnacles we were unable to obtain enough individuals in this size class for the experiments. It is plausible that prey identity influenced the observed absolute predation rates or even the shape or the peak of the measured temperature-predation functions. An additional study limitation is the potential effects of the temperature treatments on prey behavior, palatability, or even structural characteristics that could have influenced the observed temperature-specific predation rates. We did not explicitly account for these potential confounding effects, although it is incorporated into the measured response variable which is based on the net effects of temperature on both predators and their prey. It would be valuable to separate these component effects in a future study, particularly for multiple prey species. Clearly, our results are dependent on the context of the experimental design and are likely not indicative of other conditions, species, or systems. To gain a more general understanding of response diversity (and more fundamentally the temperature-dependence of predation and other ecological functions) we need far more studies in other contexts and systems. For example, given the high degree of spatiotemporal variation in temperature observed in the Galápagos it might not be surprising to observe a relatively large degree of variation in thermal tolerance among species within a functional group. But how much variation in functional response diversity is there in less variable systems, such as on equatorial reefs or in deep sea habitats?
We also estimated the thermal optima (Topt) of respiration in respirometry chambers as an indicator of the metabolic responses of each predator to warming. Topt for respiration ranged from 22ºC for Heliaster to nearly 40ºC for Vasula (Fig 4B). More important than the specific values, the respiration Topt rankings correspond closely to the relative scaling of predation rate with temperature: Tribulus and Vasula had far higher respiration Topt values than Hexaplex, and especially Heliaster (Fig 4B). Respiration rates also mirrored the same patterns across species (Fig 4A) in relation to Topt and predation rates. This suggests that the observed variation in the temperature-dependence of functional performance is related to (possibly mechanistically) species-specific metabolic sensitivity to temperature. It is often implicitly assumed, if rarely demonstrated, that measured physiological sensitivity to warming is indicative of the relative temperature-dependence (e.g., among species) of other organismal rates (e.g., growth, movement, consumption, etc.). Our results suggest that, at least for these functions and species, the relative thermal sensitivity of metabolism is predictive of the relative sensitivity of the ecological functions species fulfill in communities (that are typically much more difficult to measure).
The Galápagos marine ecosystem is noted for its highly dynamic thermal conditions [23](Fig 3). The implication of this variability for the performance of ectothermic organisms is that most species will only function near their Topt for a relatively small proportion of the thermal conditions they experience. Our results suggest that predation by the two cold-adapted species (Hexaplex and Heliaster) would be negligible when habitat temperature was above ~25ºC (Fig 4C), such as during the warm months of La Niña years (e.g., in March of 2021 and 2022, Fig 3) and for most of the year under El Niño conditions (e.g., from April 2023 to March 2024, Fig 3). In fact, during the most recent El Niño, benthic seawater temperatures exceeded the observed predation Topt of Hexaplex and Heliaster 98% and 83% of the time, respectively (Table A in S1 Text). Conversely, predation by the two experimental species most tolerant of higher temperatures (Tribulus and Vasula) should be minimal when environmental temperatures are below ~20–22ºC (Fig 4C) — much of the year under La Niña conditions (Fig 3, Table A in S1 Text). This implies that the diverse responses to temperature facilitate continued predation over a broader range of thermal conditions, ensuring functional continuity even when the performance of individual species is low.
Given the large degree of temporal temperature variance, the anthropogenic warming trend is more difficult to discern in the Galápagos compared to less variable regions [37]. A recent study detected ocean surface water warming of 1.2ºC (on average) for the region between 2002 and 2018 [24]. However, some regions of the Galápagos have warmed at nearly twice this rate — specifically the waters around the far northern islands of Darwin and Wolf. Moreover, climate models project substantial near-future warming, especially under the high emissions SSP5-8.5 scenario of CMIP6. Under these conditions, median ensemble sea surface temperatures could increase by another 2–3ºC by 2100 [38,39].
Our results indicate that warming of only a few degrees could exceed the tolerance of two of the four common invertebrate predators in our study. Both species could plausibly survive at low densities, possibly as sink populations, but would contribute little to top-down control of prey populations. However, warming could actually increase the performance of the two warm-adapted species, particularly Vasula, thereby compensating for the functional loss of Hexaplex and Heliaster. This suggests that the observed response diversity of predators and predation in this system could improve the resilience of the community to anthropogenic warming.
An important caveat is that this inference assumes little or no future adaption to natural seasonal variation in temperature or ocean warming due to greenhouse gas emissions. Marine invertebrates are clearly able to increase their thermal tolerance via adaptation, acclimatization, and other adaptive mechanisms [40–42], although most do not appear to be doing so fast enough to keep up with environmental change. Adaptation could enable species more sensitive to high temperatures to maintain functioning as the system warms, to some degree alleviating the benefits (or necessity) of response diversity. A related caveat is that our experiment exposed predators to different temperatures for 7-21 days. In the context of ocean warming, this acute temperature treatment mimics the anthropogenetic heat waves, but not necessarily the longer-term (decadal) warming trend.
The fingerprint of greenhouse gas emissions and global warming is complex in some regions of the Galápagos. For example, Fernandina and Isabela Islands, the western-most portion of the Galápagos Islands, has cooled rapidly due to the strengthening (possibly anthropogenic) of the Equatorial Under Current [24,43]. Thus, recent and possible near-future changes in the marine thermal environment of the Galápagos range from rapid cooling to extreme warming. Given these opposing temperature trends, a high degree of thermal response diversity — including the presence of cold-adapted species that will thrive in the western Galápagos with continued cooling — appears crucial to maintain functioning, and not just in warming areas. A diversity of organismal responses to temperature (essentially a broad range of largely non-overlapping thermal niches within a given functional group) can lead to the maintenance of predation across a complex and variable thermal seascape.
In summary, our results demonstrate the value of functional response diversity, and the importance of conserving species expected to fill crucial roles in a warmer world. A diversity of responses to marine heat waves in which species more tolerant of higher temperatures can functionally compensate for declines in cold-adapted species can increase ecosystem resilience to environmental change [13]. A growing body of work is beginning to suggest that community characteristics like functional response diversity are better predictors of ecological resilience than more traditional measures of biodiversity like species richness [11,13]. Untangling the relationship between ecosystem resilience to global warming and trait diversity should be a priority for field ecology.
Supporting information
S1 Text.
Fig A in S1 Text. Image of La Barcaza, one of the study collection sites. Fig B in S1 Text. Photos of the experimental aquaria setup inside the GSC marine laboratory, with labeled system components. Fig C in S1 Text. Image of predation inside the experimental system. The barnacle prey are epoxied to a rock, and the whelk Hexaplex is feeding on one of the barnacles. Fig D in S1 Text. Image of the respirometry setup during a temperature incubation for Tribulus, with labeled system components. Table A in S1 Text. The percentage of days that the mean seawater temperature at our study site Cerro Mundo, off the southwestern coast of San Cristóbal, Galápagos was higher and lower than the measured temperature of maximum performance for each of the four experimental carnivores.
https://doi.org/10.1371/journal.pclm.0000652.s001
(DOCX)
Acknowledgments
We thank the Galápagos National Park Directorate for granting scientific investigation permits to conduct this research, the Galapagos Science Center for providing laboratory facilities and other support (special thanks to S. Sotamba, J. Sotamba, C. Vintimilla, A. Pila, G. Bautista), and the University of North Carolina at Chapel Hill and the Universidad San Francisco de Quito USFQ for their support of this study. We thank the divers and field assistants who participated in the collection of organisms: S. A. Mantell, E. R. Srebnik, C. Parker, F. Rivera, N. De la Torre. We also thank boat captains Yuri Revelo and Timico Revelo and park ranger Jason Castañeda for their assistance during fieldwork and Pamela Moreno for her help with respirometry measurements. All organisms were collected under Galápagos National Park permits PC-27–22 and PC-20–23 to MB and JFB.
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