DOI: 10.5061/dryad.j3tx95xp8
title: Data from: Eat more, often: The capacity of piscivores to meet increased energy demands in warming oceans

description: Marine heatwaves (MHWs) profoundly disturb tropical coral reefs,
 imperilling species fitness and survival. Ectothermic piscivorous reef
 fishes are particularly vulnerable to MHWs since all aspects of their
 survival are dictated by ambient temperature. Severe +4°C MHWs are
 projected to escalate daily energy demands by ~32-55%, compelling
 piscivores to pursue larger or more frequent prey to survive. However, the
 feasibility of these responses have been questioned, as evolved predation
 and digestive strategies are constrained to specific prey types and sizes
 to safeguard residual aerobic scope (AS) during digestion for other vital
 processes. Instead, prevailing theory proposes appetite reductions at
 temperatures above optimal, preserving AS at the expense of growth and/or
 fitness. We investigated this dichotomy in the thermal foraging responses
 of Arc-eye hawkfish (Paracirrhites arcatus) and blacktail snapper
 (Lutjanus fulvus), evaluating energetic demand (standard metabolic rate,
 SMR), AS, appetite (meal mass intake), and capacity for digestion
 (specific dynamic action, SDA). Spanning a thermal gradient encompassing
 present-day winter (24.0±0.1°C), summer (27.5±0.1°C), and MHW
 (31.0±0.1°C), we show that SMR increased by ~65% from winter to MHW for
 both species, while AS increased by ~31-67%. Contrary to predictions of
 reduced appetite, both species consumed ~106% larger meals, yielding a
 ~35-105% greater SDA magnitude. Surprisingly, increased appetite did not
 encroach on residual AS as both species maintained the physiological
 flexibility to process larger meals while retaining ~45-60% of AS at the
 post-prandial peak. Although larger meals take longer to digest, both
 species exhibited faster digestion with rising temperatures resulting in a
 maintained or shortened SDA duration during MHWs, simultaneously enabling
 increased feeding rates while preserving aerobic reserves to support
 heightened predation. Our findings underscore the physiological
 feasibility of increasing appetite for some piscivores, while highlighting
 the ecological challenge of increasing prey numbers and sizes amid
 declining prey densities and prey size-reductions caused by ocean warming.
description: <strong><em>Study species, collection and holding
 conditions</em></strong> Arc-eye hawkfish
 (<em>Paracirrhites arcatus</em>) and blacktail snapper
 (<em>Lutjanus fulvus</em>) were selected for this study. Both
 species adopt a ‘feast and famine’ approach to foraging (i.e.,
 intermittently consume single large meals consisting of fish, crustaceans
 or other invertebrates), are from evolutionary distinct lineages
 (Cirrhitidae and Lutjanidae, respectively), and are found in high
 abundance on shallow water reefs throughout the equatorial Pacific
 (Armstrong & Schindler, 2011; Randall, 1998; Sheppard et al.,
 2017). Fish were collected with hand nets and barrier nets by scuba divers
 during the winter (January-March) and summer (July-September) of 2021 and
 2022 from reefs around Kāneʻohe Bay on the eastern coast of Oʻahu, Hawaiʻi
 (main collection site for L. fulvus: 21.414234, -157.784047 and P.
 arcatus: 21.477181, -157.791538). Following collection,
 fish were transported to the Johansen Fish Resilience Laboratory at Moku o
 Loʻe in Kāneʻohe Bay, and housed in groups of four individuals in large
 conical holding tanks (height: 86.0 cm; diameter: 82.5 cm; volume: 260 L)
 containing sections of PVC pipe for shelter. Tanks were supplied with
 flow-through, filtered, aerated and UV-sterilized seawater and subjected
 to a 12hr:12hr light:dark photoperiod. Water within the holding tanks were
 maintained at 24.0±0.1°C and 27.5±0.1°C during the winter and summer,
 respectively, reflecting mean seasonal sea surface temperatures (SST) of
 Kāneʻohe Bay (data retrieved online from tidesandcurrents.noaa.gov; Moku o
 Loʻe weather station; ID: 1612480; depth = 1 m; 21.433° N, 157.786° W).
 Water temperature within each tank was regulated using temperature control
 relays (WH1436, Willhi, China) that activated to either heat or cool the
 tank when water temperatures were not within the desired range. Heating
 within each tank was achieved with an 800 W aquarium heater (TH-08005,
 Finnex Inc., USA), whereas cooling was achieved with a submersible pump
 (D08V045CD, Kedsum, China) that circulated water from within the tank
 through a stainless-steel coil that was submerged in a 95 L external
 reservoir held at 5°C by a water chiller (ECO-1 1/2HP, Ecoplus,
 USA). Fish were allowed one week to acclimate to
 laboratory conditions and were then subjected to a ‘treatment’ for two
 weeks (see Treatment groups below). During this time, fish were fed to
 satiation on a daily basis with ~0.2-1.0 g pieces of Pacific squid
 (<em>Loligo opalescens</em>). Animal care and all of the
 experimental procedures described below complied with the ethical
 standards of the Institutional Animal Care and Use Committee at the
 University of Hawaiʻi at Mānoa, approved under the permit number
 3200. <strong><em>Treatment
 groups</em></strong> Fish collected in
 winter were assigned to the ‘winter’ treatment, whereas fish collected in
 summer were randomly assigned to either the ‘summer’ or ‘MHW’ treatment.
 Following acclimation to laboratory conditions all fish were exposed to a
 two-week trial. Specifically, fish in the winter and summer treatments
 were held at mean winter and summer SST for two weeks (i.e., 24.0±0.1°C
 and 27.5±0.1°C, respectively), while fish in the MHW treatment were held
 at mean summer SST for one week before being subjected to a simulated MHW
 for one week. A simulated MHW in this study was defined as a discrete,
 prolonged warm water anomaly above the climatological mean with a minimum
 duration of five days (following Hobday et al., 2016). Based on the
 characterization of MHWs in Kāneʻohe Bay between 1994-2020 (Tran &
 Johansen, 2023), MHWs were simulated by increasing water temperature
 ~0.9ºC per day from mean summer SST to the peak of the MHW (31.0±0.1°C),
 whereafter water temperatures were maintained at the peak of the MHW for
 at least three more days. These conditions closely matched the mean
 duration (days), maximum heating rate (°C day-1), and maximum intensity
 (°C) for MHWs detected on the reefs within Kāneʻohe Bay, ensuring that MHW
 simulations followed real-world conditions (Tran & Johansen,
 2023). Based on pilot trials, all fish were fasted during the final three
 days of the treatment period to avoid the confounding effects of specific
 dynamic action on pre-prandial whole-animal aerobic metabolic rates
 (Secor, 2009). <strong>Intermittent-flow
 respirometry</strong> Oxygen uptake rates (ṀO2)
 of <em>P. arcatus</em> and <em>L. fulvus</em> were
 measured using best practices for intermittent-flow respirometry (Clark et
 al., 2013; Roche et al., 2013; Svendsen et al., 2016). Specifically,
 respirometry trials were conducted in a temperature-controlled room
 containing two experimental tanks (length: 97 cm, width: 53 cm, height: 37
 cm) supplied with flow-through, filtered, aerated and UV-sterilized
 seawater under a 12hr:12hr light:dark photoperiod. Water temperature
 within the experimental tanks were maintained within 0.1°C of winter,
 summer, and peak MHW treatment temperatures. Each experimental tank
 contained either two large cylindrical acrylic respirometers for L. fulvus
 (length: 22.0 cm, diameter: 10.0 cm, volume: 1.600 L) or four smaller
 respirometers for P. arcatus (length: 10.6 or 14.6 cm, diameter: 3.8 or
 3.8 cm, volume: 0.166 or 0.214 L for small and large individuals,
 respectively). To feed fish within the respirometer, a 1 cm hole was
 drilled into the top of the anterior end of the respirometer, which was
 sealed with an oxygen impermeable rubber stopper when obtaining
 ṀO2 measurements. Water was continuously circulated through each
 respirometer using an in-line submersible pump (AD20P-1230E, DollaTek,
 USA) within a recirculation loop to ensure a homogenous concentration of
 oxygen throughout the respirometer. Automated flush pumps intermittently
 refreshed the water within each respirometer according to specific flush
 cycles (see Experimental protocol) set in the AquaResp software
 (v3.04, https://github.com/bigb8/AquaResp. This ensured that oxygen levels in the respirometers always remained above 80% air saturation. The partial pressure of oxygen in the water within each respirometer was measured continuously at 1 Hz using a fiber optic oxygen sensor mounted in the recirculation loop where the flow is sufficient to ensure a rapid response time of the sensor. The optode was connected to a 4-channel Firesting Optical Oxygen Meters (Pyro Science, Germany), which in turn were connected to a PC that logged the data. Oxygen measurements were automatically compensated for temperature (via a Pt100 temperature probe connected to the temperature port of the oxygen meter) and salinity (via manual input of water salinity into the Firesting logger software). Mass-specific ṀO2 were then automatically calculated by the AquaResp software from the linear decline in the partial pressure of oxygen during the measurement period when the flush pumps were off. Only ṀO2 calculations with an R2 of greater than 0.95 were kept for further analysis. <strong><em>Experimental protocol</em></strong> Following the treatment period, the experimental protocol consisted of initially determining pre-prandial whole-animal aerobic metabolic rates such as maximum metabolic rate (MMR, day 1) and SMR (days 2-3), and then subsequently determining post-prandial whole-animal aerobic metabolic rates to evaluate SDA (days 4-6) for each fish. To determine MMR, fish were individually transferred from their treatment tank to an identical tank with a reduced water level (~15 cm) and subjected to a ‘chase protocol’ (Clark et al., 2013; Norin & Clark, 2016; Roche et al., 2013). This protocol consisted of chasing the fish by hand for three minutes followed by a period of air exposure for one minute during which they were weighed and measured. Fish were then placed into respirometers and ṀO2 were obtained overnight with the AquaResp software set to ‘MMR mode’ (i.e., ‘Wait’ = 0.5 min, ‘Measure’ = 1 min, and ‘Flush’ = 2.5 min). Then to determine SMR, ṀO2 measurements were obtained for 48 h starting the following day at 07:00 HST with the AquaResp software set to ‘SMR mode’ (i.e., ‘Flush’ = 5 min, ‘Wait’ = 1 min, and ‘Measure’ = 1 min). Following the evaluation of pre-prandial whole-animal aerobic metabolic rates, fish were fed inside the respirometers by gently removing the rubber stopper from the hole in the respirometer and inserting ~0.2-1.0 g pieces of Pacific squid until the individual was satiated. Fish were deemed to be satiated when a piece of squid within the respirometer was not consumed within 15 min, whereafter unconsumed pieces of squid were gently removed and the respirometer was re-sealed with the rubber stopper. The feeding process typically took ~30 min. To determine SDA, post-prandial ṀO2 measurements were then obtained for another 72 h with the AquaResp software set to ‘SMR” mode. At the end of the experiment, fish were removed from the respirometers for subsequent release back into the wild at the approximate location of capture. To account for background respiration, linear regression over time using measures of bacterial ṀO2 obtained from empty respirometers before and after each respirometry trial were subtracted from all ṀO2 measurements. To limit background respiration rates, all equipment was disinfected with a 1% bleach solution, thoroughly rinsed with freshwater, and allowed to dry before commencing further trials. <strong><em>Determining pre-prandial responses</em></strong> A total of 44 individual <em>P. arcatus</em> (n: winter=14, summer=17, MHW=19) and 35 <em>L. fulvus</em> (n: winter=11, summer=12, MHW=12) were used to determine pre-prandial metabolic rates. MMR was defined as the highest pre-prandial <em>Ṁ*O2 measurement (Norin & Clark, 2016, 2017), while the 20% quantile method on *Ṁ*O2 measurements obtained during the 48 h pre-prandial period yielded the most consistent SMR estimates based on visual inspection of *Ṁ*O2 and the cumulative variance of the mean lowest normal distribution (Chabot *et al</em>., 2016). In addition, Q10 was calculated (<em>i.e</em>., Q10 = (R2/R1)[10/(T2-T1)]) using mean SMR values for each species between winter and summer (<em>i.e</em>., R1: SMRwinter; R2: SMRsummer; T1: 24.0°C; T2: 27.5°C), as well as between summer and at the peak of a simulated MHW (<em>i.e</em>., R1: SMRsummer; R2: SMRpeak of MHW; T1: 27.5°C; T2: 31.0°C). AS was calculated as MMR minus SMR (Clark <em>et al</em>., 2013). In order to accurately quantify SDA (see Determining post-prandial responses below), it is recommended to account for the 'metabolic circadian rhythm' of the study organism to account for brief periods of spontaneous activity (Roe et al., 2004). This was achieved for each individual by calculating an hourly moving median of the ṀO2 measurements obtained during the 48 h pre-prandial period. From the smoothed data, parameters of the ‘metabolic circadian rhythm’ such as the mesor (i.e., mean of the circadian rhythm) and amplitude (i.e., difference between the mesor and peak of the ‘metabolic circadian rhythm’) were calculated for each individual. Likewise, routine metabolic rate (RMR) was calculated for each individual by subtracting SMR from the mesor of the 'metabolic circadian rhythm’ to evaluate rates of surplus energy expenditure (i.e., energetic expenditure in excess of that required for maintaining homeostasis). <strong><em>Determining post-prandial responses</em></strong> Following exclusion of individuals due to high background respiration (i.e., background respiration &gt;10% of SMR, likely due to the presence of faeces within some respirometers), noisy ṀO2 measurements (i.e., R2&lt;0.95), or lack of feeding, a total of 36 individual P. arcatus (n: winter=12, summer=14, MHW=10) and 32 L. fulvus (n: winter=10, summer=11, MHW=11) were used to determine post-prandial metabolic rates. To account for brief periods of spontaneous activity during the SDA period, an hourly moving median was applied to post-prandial ṀO2 measurements. The post-prandial response of an individual was then defined as the period of elevated ṀO2 occurring directly after feeding until post-prandial values had returned to pre-prandial levels – defined as &gt;8 consecutive smoothed post-prandial ṀO2 values (&gt;1 h of measurements) that were ≤ ‘metabolic circadian rhythm’ of that individual (i.e., median + median deviation of pre-prandial ṀO2 expected for that time of day). The accumulated energy expended from the ingestion, digestion, absorption and assimilation of a meal (SDAabsolute) was calculated from the amount of oxygen consumed above the ‘metabolic circadian rhythm’ during the entire post-prandial response, and converted to units of energy with a conversion factor of 20.083 kJ L O2-1 (Schmidt-Nielsen, 1997). The proportion of AS that was occupied by the SDA response (SDArelative) was calculated by dividing the total amount of oxygen consumed above SMR by AS during the entire post-prandial response. The absolute peak of the post-prandial response (SDAabsolute peak) was defined as the highest smoothed value of ṀO2 during the post-prandial response, and was also calculated as a percentage of AS (SDArelative peak). The duration of the post-prandial response (SDAduration) was calculated as the period of time between feeding and the completion of the post-prandial response. The efficiency of the SDA response (SDAcoefficient) was calculated by dividing SDAabsolute with the amount of digestible meal energy from Pacific squid, which was 2.510 kJ g-1 based on the nutritional information provided on the packaging (Emerald Calamari, Del Mar Seafoods, Inc., Watsonville, CA, USA) and assuming a conversion factor of 4.184 kJ kcal-1 (Schmidt-Nielsen, 1997). <strong><em>Statistical analyses</em></strong> All statistical analyses were performed using R. Detailed descriptions of the statistical analyses used for pre-prandial (i.e., SMR, MMR, AS, RMR, as well as the mesor and amplitude of ‘metabolic circadian rhythm’), prandial (i.e., meal size), and post-prandial data (i.e., SDAabsolute, SDArelative, SDAcoefficient, SDAabsolute peak, SDArelative peak, and SDAduration) are provided in the supplementary information (e.g., R packages used, data exploration, model fitting, model selection, model checking, model inference and model predictions; see Supp. Info. 1-2). Briefly, pre-prandial and prandial linear regression models were fit using various combinations of body mass, treatment temperature, and species, as well as the interactions between them (Table 1). Post-prandial linear regression models were fit using various combinations of body mass, meal size, treatment temperature, and species, as well as the interactions between them (Table 1). The best-fitting models were selected based on Akaike’s Information Criterion (AIC) and model assumptions were checked (Burnham & Anderson, 2002). All variables with the exception of treatment temperature, species and SDA duration were log transformed to meet model assumptions. The main inferences from the most parsimonious models are reported throughout the text, while back-transformed model predictions are displayed in the figures. For detailed model summary outputs and extensive model inferences refer to Table 1 and Supp. Info. 1-2, respectively. Planned contrasts were conducted to investigate treatment temperature differences for an average sized individual (i.e., mean body masses of 9 or 45 g for <em>P. arcatus</em> or <em>L. fulvus</em>, respectively) and/or meal size (i.e., mean meal sizes of 0.53 or 3.63 g for <em>P. arcatus</em> or *L. fulvu*s, respectively) for each species. The p-values resulting from the planned contrasts were subjected to False Discovery Rate (FDR) adjustment using the Benjamini-Hochberg procedure to account for multiple testing (Benjamini & Hochberg, 1995).
description: # Data from: Eat more, often: The capacity of piscivores to meet increased
 energy demands in warming oceans
 [https://doi.org/10.5061/dryad.j3tx95xp8](https://doi.org/10.5061/dryad.j3tx95xp8) ## Key for data set **Pre-prandial data set:** -ID: identification number assigned to each individual based on species and treatment -Species: 1 = Arc-eye hawkfish (*Paracirrhites arcatus*), 2 = blacktail snapper (*Lutjanus fulvus*) -Treatment: 1 = present-day winter (24.0±0.1°C), 2 = summer (27.5±0.1°C), and 3 = peak of simulated MHW (31.0±0.1°C) -Mass/lnMass: represents wet weight of each individual -SMR/lnSMR: represents the standard metabolic rate of each individual -MMR/lnMMR: represents the maximum metabolic rate of each individual -AS/lnAS: represents the aerobic scope of each individual -MesorCirc/lnMesorCirc: represents the mesor of the circadian metabolic rhythm of each individual -AmpCirc/lnAmpCirc: represents the amplitude of the circadian metabolic rhythm of each individual -RMR/lnRMR: represents the routine metabolic rate of each individual **Post-prandial data set:** -ID: identification number assigned to each individual based on species and treatment -Species: 1 = Arc-eye hawkfish (*Paracirrhites arcatus*), 2 = blacktail snapper (*Lutjanus fulvus*) -Treatment: 1 = present-day winter (24.0±0.1°C), 2 = summer (27.5±0.1°C), and 3 = peak of simulated MHW (31.0±0.1°C) -Mass/lnMass: represents wet weight of each individual -Mealsize/lnMealsize: represents wet weight of the meal each individual consumed -Relativemealsize/lnRelativemealsize: represents wet weight of the meal each individual consumed in proportion to body mass -peakSDA/lnpeakSDA: represents the peak postprandial metabolic response for each individual -SDAscope/lnSDAscope: represents peak postprandial metabolic response divided by standard metabolic rate for each individual -Duration/lnDuration: represents the duration of the entire postprandial metabolic response for each individual -SDA/lnSDA: represents the specific dynamic action or the sum of the entire postprandial metabolic response for each individual -SDAcoeff/lnSDAcoeff: represents the efficiency of the postprandial metabolic response for each individual -RMR/lnRMR: represents the routine metabolic rate of each individual -RelativepeakSDA/lnRelative peakSDA: represents the peak postprandial metabolic response for each individual in proportion to their aerobic scope -RelativeSDA/lnRelativeSDA: represents the sum of the entire postprandial metabolic response for each individual in proportion to their aerobic scope ## Usage notes Requires Microsoft Excel