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A global meta-analysis of temperature effects on marine fishes’ digestion across trophic groups

Citation

Knight, Nicole; Guichard, Frederic; Altieri, Andrew (2021), A global meta-analysis of temperature effects on marine fishes’ digestion across trophic groups , Dryad, Dataset, https://doi.org/10.5061/dryad.g1jwstqq1

Abstract

Aim: The temperature constraint hypothesis proposes that marine herbivorous fishes are rare at high latitudes relative to carnivorous fishes because low temperatures impair the digestion of plant material. To test this hypothesis, we compared the effects of temperature on the digestive performance and investment of marine fishes across trophic groups.

Location: Global marine ecosystems.

Major Taxa Studied: Marine fishes.

Methods: We analyzed data from 304 species consuming a range of diets to quantify the effects of temperature on three indicators of digestive performance and investment: gut passage time, absorption efficiency, and gut length.

Results: Decreasing temperatures increase gut passage time in fishes consuming macroalgae more than fishes consuming other fish or invertebrates. Low temperatures do not impair absorption efficiency in fishes regardless of diet, but herbivores have lower absorption efficiencies than carnivores overall. Gut length decreases with decreasing temperature in all trophic groups.

Main Conclusions: Our analyses reveal limited evidence to support the temperature constraint hypothesis.  Low temperatures slow digestion more in fishes consuming macroalgae than those consuming animal prey; however, this may not reflect a meaningful disadvantage for herbivores but rather could be explained by greater representation of fishes relying on microbial fermentation at high latitudes.  Herbivorous fishes absorb nutrients and energy from their food in similar proportions regardless of temperature, contrary to the expectations of the temperature constraint hypothesis.  Decreased gut length was associated with decreasing temperature across all trophic groups, likely due to improved food quality at high latitudes, which should benefit all trophic groups by reducing their required investment in gut tissues. Altogether, our findings run counter to the general hypothesis that low temperatures disadvantage the digestion of plant material and suppress the diversity and abundance of herbivorous fishes at high latitudes.

Methods

Literature search and data collection

Eligibility criteria

For an estimate of gut passage time, absorption efficiency or gut length to be included in our meta-analysis it had to have the following characteristics:

  1. Taken from marine or estuarine fish species
  2. Taken from non-larval individuals
  3. Not taken from species that are strictly detritivorous or corallivorous
  4. Not taken from individuals fed an artificial diet with optimized composition for nutrient uptake/digestion (i.e., as found in many aquaculture studies)
  5. Not taken from individuals force-fed food items not typically consumed in the wild

and

  1. In the case of gut length, reported some metric of body length or size.

We note that there exists a large body of literature on the “gastric evacuation rates” (the rate at which food leaves the stomach and enters the hindgut) of carnivores, which was developed as a method for indirectly estimating feeding rates by quantifying the minimum amount of time required for stomach clearance between meals (Bromley, 1994).  We chose not to include this data in our analysis because: a) almost no data on gastric evacuation rates exists for herbivores so we could not make valid comparisons between trophic groups, and b) gastric evacuation rates have been estimated using a wide range of methods and models, and it is unclear under what circumstances comparisons between such models is meaningful (Bromley, 1994).  Gut passage time has been quantified for both herbivores and carnivores and is a more easily comparable metric.

Information sources and search

We searched Web of Science, JSTOR, and Google Scholar.  We also included data that were found in relevant review papers and in publications that cited, or were cited in, the papers discovered in our database search, as well as relevant papers found incidentally.  Altogether, we included papers published between 1958 and March 2020.  All search term combinations included marine and fish, as well as the following combinations of additional search terms (but not all search term combinations were used for all databases): assim*, assimilation eff*, absorption, absorption eff*, “absorption efficiency”, “assimilation efficiency”, excret*, egest*, conversion, “gut length”, “gut morphology”, gut passage, gut transit, “gut passage time”, “gut transit time”, digest*,  digest* + temperature.  We initially excluded studies if their titles or abstracts were not relevant, then checked the remaining studies for data that met the eligibility criteria described above.  By the end of this process, 99 studies were eligible for inclusion in the meta-analysis.              

Data collection

Data were extracted from text, tables, and figures in the accepted studies.  We collected temperature and diet as predictor variables, as well as body length, since many biological traits scale with size (Brown et al., 2004).  However, metrics of body size in reported in collected studies varied widely.  Metrics included standard length, total length, and fork length, these were further divided into average values, median values, maximum/minimum values, or no reported values.  Whenever possible, we used the average body size; if this was not provided, we used the mid-range (maximum – minimum / 2) body size provided.  We did not distinguish between standard, total and fork length.  If fish mass but not length was reported, we used published length-weight relationships for the species in question to calculate fish length.  These instances are noted in the raw data.

Ambient temperature was likewise not always included in all the studies included in our dataset, particularly for estimates of gut length. We supplemented these datasets by extracting the date and location of data collection from the study, and used that data to find the local sea surface temperature (SST) at the time of sampling from the COBE SST data provided by NOAA/OAR/ESRL PSD via http://www.esrl.noaa.gov/psd/. On the rare occasion that the specific collection period was not included in the publication, we took the average temperature of the location for five years preceding publication of the data. These instances are noted in the data.

Usage Notes

See README.txt.

Funding

Natural Sciences and Engineering Research Council of Canada

McGill University

Smithsonian Tropical Research Institute