Ecological Archives E094-108-D1

Anthony I. Dell, Samraat Pawar, Van M. Savage. 2013. The thermal dependence of biological traits. Ecology 94:1205. http://dx.doi.org/10.1890/12-2060.1


Introduction

Because environmental temperature has pervasive effects across cells, individuals, populations, and ecosystems, elucidating mechanisms by which biological systems respond to temperature is essential for understanding how these systems operate in nature. Given rapid changes to Earth’s thermal environment (IPCC 2007), understanding species’ thermal responses and their consequences for biodiversity and ecosystem functioning is especially critical (Petchey et al. 2010, Rall et al. 2010, Dell et al. 2013).

Body temperature, a major driver of individual physiology from cellular respiration to whole organismal respiration, is strongly affected by environmental temperature in ectotherms (Johnson et al. 1974, Cossins and Bowler 1987, Huey and Kingsolver 1989, Somero , Gillooly et al. 2001, Brown et al. 2004, Angilletta 2009, Dell et al. 2011). These individual-level effects cascade up to affect populations, species interactions, and ecosystems. An understanding of how these effects translate across levels of biological organization requires analysis of a broad suite of functional traits spanning from cells to communities (Angilletta 2009, Dell et al. 2011). For nearly a century, intraspecific studies, which measure a trait within a single species’ population across a range of temperatures, have been conducted on a variety of biological traits (e.g., Bennett 1980, Hertz et al. 1982, Cossins and Bowler 1987, Gillooly et al. 2002, Savage et al. 2004, Ratkowsky et al. 2005, Frazier et al. 2006, Angilletta 2009, Irlich et al. 2009b). However, comparative studies of these intraspecific data have tended to focus on small subsets of available data (e.g., Huey and Bennett 1987, Huey and Kingsolver 1989, Bauwens et al. 1995, Huey and Berrigan 2001, Irlich et al. 2009b), probably for two central reasons. First, there is clearly a general lack of empirical data on the thermal response of ecological traits required to address particular ecological and evolutionary questions. This issue must be addressed by a renewed effort by empirical biologists to collect more thermal response data on traits relevant to species interactions. Second, there is a lack of a comprehensive database that compiles existing data, which is required to compare methodologically and taxonomically diverse thermal response data.

In this paper we address the second issue by constructing from published sources a data set that contains 2352 intraspecific temperature responses. This data set is the most comprehensive ever compiled for the thermal responses of physiological and ecological traits. We emphasize that this database focuses mainly on “ecological traits”, which we define here to mean any organismal trait that directly determines or measures interactions between individuals within or between species. Our effort was motivated by the fact that understanding effects of global warming on species interactions is one of the major challenges in contemporary ecology (Harrington et al. 1999, Walther et al. 2002, Helmuth et al. 2005, Vasseur and McCann 2005, Woodward et al. 2010, Dell et al. in print). The resulting global database contains intraspecific thermal responses for 220 traits and 411 species of plants, microbes, and animals that span 16 orders of magnitude in body size. This is also the first compilation of organismal thermal responses wherein all traits have been converted to consistent units and standardized trait definitions.

Analysis of this data set should reveal how biological systems respond to temperature (Irlich et al. 2009a, Dell et al. 2011, Englund et al. 2011, Nilsson-Örtman et al. 2012). These intraspecific data can also be used to investigate interspecific thermal response curves, which are constructed from trait measurements for multiple species at their optimal temperature and plotted together to construct a single curve (Brown et al. 2004, Angilletta 2009, Dell et al. 2011) . Patterns of interspecific thermal response curves are important because they represent underlying constraints on thermal adaptation (Gillooly et al. 2001, Gillooly et al. 2002, Izem 2005, Frazier et al. 2006, Knies et al. 2009, Angilletta et al. 2010, Corkrey et al. 2012). This data set should also be useful in testing assumptions and predictions of mechanistic models, such as the metabolic theory of ecology (Gillooly et al. 2001, Gillooly et al. 2002, Brown et al. 2004). Ultimately, we hope analysis of this comprehensive data set will illuminate previously unrecognized generalities and deviations in how biological systems respond to temperature (Dell et al. 2011), and help elucidate the mechanisms by which life responds to Earth’s complex and rapidly changing thermal landscape.

Metadata

Class I. Data set descriptors

A. Data set identity: Compilation of published intraspecific thermal response curves for physiological and ecological traits.

 

B. Data set identification code: TempTrait_001.txt

C. Data set description

Summary: Data set has 19,921 records from 2,352 intraspecific temperature response curves that measure the thermal dependence of physiological and ecological traits from 411 taxa and various marine, terrestrial and freshwater habitats. Each record has 65 fields that detail the trait, taxa, and experimental conditions of each thermal response.

Principal Investigators: Anthony I. Dell, Systemic Conservation Biology, Department of Biology, Georg-August University Göttingen, Göttingen 37073, Germany; Samraat Pawar, Department of Ecology & Evolution, University of Chicago, Chicago, IL 60637, USA; Van M. Savage, Department of Biomathematics, UCLA School of Medicine, Los Angeles, CA 90024, USA. Queries regarding the data set should be directed to A.I. Dell (adell@gwdg.de).

Abstract: Environmental temperature has strong and systematic effects on biological processes at all levels of organization, ranging from cells to ecosystems. The large temporal and spatial variation in earth’s temperature creates a complex thermal landscape within which life evolves and operates. Here, we present a data set on how diverse biological rates and times respond to temperature, which we hope will aid in the search for general mechanisms of thermal dependence. For nearly a century, intraspecific studies (within single species’ populations) of thermal responses have been conducted on a wide range of organismal traits. Comparative studies of these data are essential for elucidating mechanisms underlying thermal response curves. However, such comparative intraspecific studies have been limited because of a lack of a comprehensive database that organizes these data with consistent units and trait definitions. Here, we present a database of 2352 thermal responses for 220 traits for microbes, plants, and animals compiled from 270 published sources. This represents the most diverse and comprehensive thermal response data set ever compiled. The traits in this database span levels of biological organization from internal physiology to species interactions, and were measured in marine, freshwater, and terrestrial habitats for 411 species. Although we include some physiological rates, most data are for ecological traits, which we define here to mean any organismal trait that directly determines interactions between individuals within or between species. We hope that publication of our data set will encourage others to compile complementary data sets, especially on individual physiology and life history traits. Intraspecific and interspecific (across species’ populations) analyses of our data set should provide new insights into generalities and deviations in the thermal dependence of biological traits, and thus how biological systems, from cells to ecosystems, respond to temperature change. Such insights are essential for understanding how natural biological systems function, and for how life is responding to Earth’s complex and rapidly changing thermal landscape.

D. Key words: database; ecoinformatics; ecology; environmental driver; evolution; interspecific; intraspecific; species; thermal response; temperature; trait.

Class II. Research origin descriptors

A. Overall project description

Identity:The thermal dependence of biological traits.

Originators: Anthony I. Dell, Samraat Pawar, and Van M. Savage.

Period of Study: Dates of publications from which data were obtained currently range from 1923 to 2009.

Objectives: The objective of this project was to construct a comprehensive and consistent data set of measurements of the thermal dependence of a wide range of physiological and ecological traits from diverse taxa and habitats. Such a single, extensive data set for multiple traits with consistent measurement units and trait definitions should facilitate novel comparative analyses and hypothesis testing, yielding new insights into generalities and important deviations in thermal responses of biological systems. Eventually, these data should help reveal general mechanisms by which life responds to changing thermal landscapes worldwide.

Abstract: As above.

Sources of funding: University of California Los Angeles (Biomathematics); National Science Foundation Division of Environmental Biology (1021010); James Cook University (Tropical Biology), Australian Research Council.

B. Specific subproject description

Data Acquisition. We searched the published literature for intraspecific thermal response curves on biological traits, with a primary focus on traits central to species interactions. The temperature response of traits can be strongly influenced by organismal behavior (e.g., Schieffelin and Dequeiroz 1991, Cooper 2000, Shine et al. 2000, Herrel et al. 2007). Therefore, we focused on rates and times of the execution of biological processes (e.g., attack body velocity, handling rate) and not on decisions about whether to execute them (e.g., attack probability, defense behavior probability). In total, we found 270 data sources that described intraspecific thermal responses, including journal articles, published reports, and books. We attempted to contact authors directly to obtain raw data, but if this was not possible we extracted data directly from tables and text or from figures using DataThief (Tummers 2006). Our use of DataThief made it impossible to know the true precision of the original data. Also, because we sometimes obtained raw data from the authors, in some cases our data set will not exactly match that described within the original publication (e.g., replicate thermal responses are not combined). This procedure yielded 2352 intraspecific temperature responses and 19,921 data points. We primarily selected studies where environmental conditions, such as precipitation, light, and prey density were either controlled or standardized. Consequently, most responses were measured in the laboratory, where ectotherm body temperatures were known to be close to ambient (based on direct measurements and extended acclimation times at test temperatures). The 270 sources from which data were described and analysed in this paper are listed in the Citations field of the data file. Because the number of studies on thermal responses of ecological traits is increasing rapidly, we are currently adding to the data set, which will be updated periodically.

Unit Conversions. Definitions and measures of many traits are inconsistent throughout the literature, so we identified equivalent traits and converted them to comparable definitions and SI units. Where possible, probabilistic trait data were converted to rates or times.

Taxonomy and systematics: Taxonomic designations were used as stated in the source publication, unless there was clear evidence of a name change in which case the new name was used. Each species’ taxonomic hierarchy was determined by using Species 2000 (http://www.sp2000.org), the Encyclopedia of Life (http://eol.org), and Animal Diversity Web (http://animaldiversity.ummz.umich.edu).

Body Size. When available, wet mass of each organism was obtained from the original data source. For studies in which body mass was not provided, we developed an algorithm that assigned a wet mass estimate to species in each data row. This algorithm was based on taxonomic relatedness to published size estimates and length-mass regressions, and allowed us to rapidly obtain estimates of wet body mass that well matched published measurements. Details of the algorithm and its implementation are given in Dell et al. (2011).

Permit history: N/A.

Legal/organizational requirements: None.

Project personnel: Anthony I. Dell, Samraat Pawar, and Van M. Savage.

Class III. Data set status and accessibility

A. Status

Latest update: August 2012. Data compilation is ongoing and will be added as collected and verified.

Latest Archive date: August 2012.

Metadata status: Metadata are complete and up to date.

Data verification: A. I. Dell, with assistance from S. Pawar, entered records directly from original sources into MS Access. All values were at minimum triple checked at various stages of data complication and analysis. Plots of each thermal response were automatically produced in MS Access and compared to figures in the original source. In addition, outliers in numeric variables were sorted to examine extreme values. For body size estimates (Class II, Section B) we constructed box plots by taxonomy (Family and Order) and observed outliers for errors. It is important to note that in cases where we obtained raw data directly from authors (see above) our data will not exactly match that described within the original publication, because our data will be more detailed (e.g., replicates are not averaged).

B. Accessibility

Storage location and medium: The data set is available from the Ecological Society of America’s data archives. A digital version of the dataset in MS Excel format is held by A. I. Dell, and a beta mySQL version (searchable by trait, taxa, and citation) is now available online at www.biotraits.ucla.edu.

Contact person: Anthony I. Dell, Systemic Conservation Biology, Department of Biology, Georg-August University Göttingen, Göttingen 37073, Germany (adell@gwdg.de).

Copyright restrictions: None.

Proprietary restrictions: None, except this data paper, NSF Division of Environmental Biology Award 1021010, and the website (www.biotraits.ucla.edu) should be cited when the data are used for a publication. In addition, we would appreciate hearing which research questions or teaching exercises the data are being used for.

Costs: None.

Class IV. Data structural descriptors

A. Data Set File

Identity:TempTrait_001.txt

Size:19,921 records (including header) and 65 fields. Total file size is 17.8 mb.

Format and storage mode: UncompressedUTF-16 text, tab delimited.

Header information: The first row of the file contains variable names (see below).

Row information: Each row represents trait performance at a single ambient or body temperature for a single species, or combination of two species when the trait involves interactions between species (e.g., encounter or consumption rate).

Alphanumeric attributes: Mixed. Note that degree of precision (i.e., number of decimal places) in number fields does not always match the original source for two reasons. First, our data is often more detailed than in the original source because where possible we obtained raw data from the authors (e.g., replicate thermal responses are not combined). Second, our use of DataThief (Class II, Section B) made it impossible to know the true precision of the original data. For consistency all SI number fields were converted to scientific notation floating point (Table 1).

Special characters/fields: Missing data denoted as NA.

Authentication procedures: Only data from published literature were obtained, although in a few cases we included other associated data offered by authors that we contacted about their published data. Field sums for all numeric fields are listed in the Authen field (Table 1) and should be used to authenticate the accuracy of the data.

B. Variable information

Variables and their details are provided in Table 1. Further details about variables are given in Dell et al. (2011).

Table 1. Summary of variable information. "Authen" represents the sum of that numeric field (i.e., all rows) rounded to closest integer, and should be used to authenticate the contents of the data file.

Variable

Variable definition

Type

Variable codes

Authen

DataSeriesID

Unique identifier code for each intraspecific thermal response curve

Integer

NA

634618613

 

Trait

Trait name

Character

NA

NA

TraitDef

Trait definition

Character

NA

NA

TraitOrg

Level of biological organization of the trait

Character

internal = processes internal to the organism; individual = processes at the level of individual organisms that include mechanical interactions with the external environment; population = processes for a group of conspecific individuals; interaction = processes involving interaction between two or more species

NA

AmbientTemp

Temperature (°C) of ambient environment (i.e., field or experimental arena).

Floating point

If null (NA) then see ConTemp or ResTemp

404934

TraitValueSI

Value of trait performance in SI units

Floating point

NA

523272551

TraitUnitSI

Units for trait performance in SI units

Character

NA

NA

ErrorPosSI

Positive value of error in SI units (see ErrorUnitSI)

Floating point

NA

26230188

 

 

ErrorNegSI

Negative value of error in SI units (see ErrorUnitSI)

Floating point

NA

25702176

 

ErrorUnitSI

Unit of error

Character

SD = standard deviation; SE = standard error; 95% CI = 95% confidence interval; interquartile range; range

NA

Replicates

Number of replicates for each record

Integer

NA

145002

 

Habitat

Habitat where trait performance was measured

Character

terrestrial; freshwater; marine

NA

LabField

Whether trait performance was measured in the laboratory or field

Character

laboratory; field

NA

ArenaValueSI

SI value of size of arena where trait performance was measured

Floating point

NA

165367

ArenaUnitSI

SI unit of size of arena where trait performance was measured

Character

cubic meter; square meter; meter = when only length of arena was stated

NA

ObsTimeValueSI

SI value of total observation time (i.e., time over which experiment was run for measurement of trait performance)

Floating point

NA

4251168740

ObsTimeUnitSI

SI unit of total observation time (i.e., time over which experiment was run for measurement of trait performance)

Character

second; prey caught = time taken for ObsTimeValueSI number of prey caught

NA

ObsTimeNotes

Notes for total observation time (i.e., time over which experiment was run for measurement of trait performance)

Character

NA

NA

ResRepValueSI

SI value for how often resources were replaced over observation time

Floating point

NA

810257360400

ResRepUnitSI

SI value for how often resources were replaced over observation time

Character

not replaced; second; to satiation = resources replaced sufficiently frequently so that consumer always had access to resources

NA

Location

Location (generally town, state, country) of where organisms were collected, or when measurements were taken at a different location then both are listed

Character

NA

NA

Latitude

Approximate latitude of middle of location where animals were collected (e.g., filed station, town, state, country), or when not available then where measurements were taken.

Numeric (3 decimal places)

NA

616917

Longitude

Approximate longitude of middle of location where animals were collected (e.g., filed station, town, state, country), or when not available then where measurements were taken.

Numeric (3 decimal places)

NA

-809413

TaxaPresent

Whether one or two taxa are part of the trait measurement and definition. If only a single organism is involved (e.g., metabolic rate, heart rate), it is always listed as a trait for a consumer.

Character

consumer = trait involves a single organism; consumer-resource = trait involves two organisms

NA

ConType

 

Type of consumer

Character

alive = organism alive when trait performance measured; dead = organism dead when trait performance measured; artificial = ‘organism’ simulated by a physical stimulus (e.g., predator model, prodding, gravity)

NA

Con

 

Binomial name of consumer or lowest taxonomic identity, or other appropriate name for artificial taxa (see ConType)

Character

NA

NA

ConCommon

Common name of consumer

Character

NA

NA

ConStage

 

Life stage of consumer, and sex in parenthesis when available

Character

NA

NA

ConIDLevel

 

Taxonomic level to which the consumer was identified

Character

kingdom, phylum, class, order, family, genus, species

NA

ConKingdom

 

Taxonomic name of Kingdom of consumer

Character

NA

NA

ConPhylum

Taxonomic name of Phylum of consumer

Character

NA

NA

ConClass

 

Taxonomic name of Class of consumer

Character

NA

NA

ConOrder

 

Taxonomic name of Order of consumer

Character

NA

NA

ConFamily

 

Taxonomic name of Kingdom of consumer

Character

NA

NA

ConTrophic

 

Broad trophic group of consumer, as determined by published literature and expert opinion

Character

carnivore; detritivore; herbivore; omnivore, producer, artificial (see ConType); self = energy self-supplied (e.g., pupae, egg); dead (see ConType)

NA

ConThermy

Thermy of consumer

Character

ectotherm; endotherm

NA

ConTemp

 

Body temperature (°C) of consumer

Floating point

NA

482173

 

ConTempMethod

 

Method of determining body temperature of consumer

Character

direct = measured directly from within or on the organism; inferred (ambient) = estimated from known ambient temperature and generally within arena where organism not able to thermoregulate; inferred (endotherm) = body temperature relatively constant and estimated from published literature; inferred (consumer) = estimated from known consumer body temperature (relevant for ResTempMethod, see below)

NA

ConMassValueSI

 

Mass of consumer as obtained from original source or estimated from other published literature (see Dell et al. (2011) for further details)

Floating point

NA

196296

 

ConMassUnitSI

SI unit of consumer mass

Character

kilogram (wet body mass) = wet mass of entire body of consumer; kilogram (wet tissue mass) = wet mass of tissue of consumer (e.g., excluding shell for gastropods)

NA

ConDenValueSI

Value of consumer density standardized to SI units

Floating point

NA

2471839374

ConDenTypeSI

Type of units of consumer density

Character

individual; kilogram (dry body mass); kilogram (wet body mass); liter; to satiation = resource density above what consumer could fully consume (relevant for ResDenTypeSI, see below)

NA

ConDenUnitSI

SI units of consumer density

Character

arena; square meter; cubic meter

NA

ResType

Same as for ConType (see above), but for resource

NA

Res

Same as for Con (see above), but for resource

NA

ResCommon

Same as for ConCommon (see above), but for resource

NA

ResStage

Same as for ConStage (see above), but for resource

NA

ResIDLevel

Same as for ConIDLevel (see above), but for resource

NA

ResKingdom

Same as for ConKingdom (see above), but for resource

NA

ResPhylum

Same as for ConPhylum (see above), but for resource

NA

ResClass

Same as for ConClass (see above), but for resource

NA

ResOrder

Same as for ConOrder (see above), but for resource

NA

ResFamily

Same as for ConFamily (see above), but for resource

NA

ResTrophic

Same as for ConTrophic (see above), but for resource

NA

ResThermy

Same as for ConThermy (see above), but for resource

NA

ResTemp

Same as for ConTemp (see above), but for resource

312208

ResTempMethod

Same as for ConTempMethod (see above), but for resource

NA

ResMassValueSI

Same as for ConMassValueSI (see above), but for resource

554

ResMassUnitSI

Same as for ConMassUnitSI (see above), but for resource

NA

ResDenValueSI

Same as for ConDenValueSI (see above), but for resource

423196940674347

ResDenTypeSI

Same as for ConDenTypeSI (see above), but for resource

NA

ResDenUnitSI

Same as for ConDenUnitSI (see above), but for resource

NA

CitationID

Unique identification number for citation

Integer

NA       

7026820

 

Citation

Citation from which data was obtained

Character

NA

NA     

FigureTable

Figure or table from which data was obtained within original citation

Character

NA

NA

 

Class V. Supplemental descriptors

A. Data acquisition

Potential data sources were identified using three methods:

  1. Using literature search engines (e.g., Web of Science, JSTOR) to find published literature using keyword combinations that included: ‘ecological’, ‘ecology’, ‘interaction’, ‘physiological’, ‘physiology’, ‘response’, ‘temperature’, ‘thermal’, and ‘trait’. In many cases, the authors of these studies were contacted directly to obtain raw data.
  2. Contacting known researchers in the field of thermal biology and directly requesting data.
  3. Looking through citations in the publications found by method 1.

Once identified, data were obtained by contacting authors and asking for raw data, otherwise directly from the main text and tables of published literature, and from figures using DataThief (Tummers 2006) that allows digitization of data points from a graph.

B. Quality assurance/quality control procedures: See comments on data verification (Class III, Section A).

C. Related material: N/A.

D. Computer programs and data processing algorithms: Data from figures in published literature were obtained with DataThief (Tummers 2006) (see Class V, Section A). Data were entered into a form within MS Access, where unit conversions to SI units were also undertaken. Body size estimates were made using an algorithm we constructed and implemented using MS Access (Class II, Section B) (Dell et al. 2011).

E. Archiving: Data files and metadata will be updated periodically at Ecological Archives, and are available in beta version at www.biotraits.ucla.edu.

F. Literature cited:

Publications from which data were obtained are stated in the Citation field of the data file.

G. Publications using the data set:

Dell, A. I., S. Pawar, and V. M. Savage. 2011. Systematic variation in the temperature dependence of physiological and ecological traits. Proceedings of the National Academy of Sciences of the United States of America 108:10591–10596.

Dell, A. I., S. Pawar, and V. M. Savage. 2013. Temperature dependence of trophic interactions are driven by assymetry of species responses and forgaing strategy. Journal of Animal Ecology. In press.

Pawar, S., A. I. Dell, and V. M. Savage. 2012. Dimensionality of consumer search space drives trophic interaction strengths. Nature 486:485–489.

Pawar, S., A. I. Dell, and V. M. Savage. 2013. Does consumption rate scale superlinearly? - Reply. Nature.

H. History of data set usage

Data request history: N/A

Data set update history: N/A.

Review history: N/A.

Questions and comments from secondary users: N/A

Acknowledgments

We sincerely thank the many authors who graciously donated their time and data. Without their careful work, the compilation of this data set would have been either impossible or meaningless. In addition, we would like to thank the many organizations that helped fund each of these projects. We thank Kina Winoto for help in porting the original data set to mySQL and, together with William King, for helping develop the website where this data set is currently being made available (www.biotraits.ucla.edu). We thank Mike Angilletta, William King, and one anonymous reviewer for their detailed and insightful comments. Support for compiling this data set was provided by James Cook University, the University of California Los Angeles, and the National Science Foundation Division of Environmental Biology Award (1021010).

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Angilletta, M. J., R. B. Huey, and M. R. Frazier. 2010. Thermodynamic effects on organismal performance: Is hotter better? Physiological and Biochemical Zoology 83:197–206.

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Bennett, A. F. 1980. The thermal-dependence of lizard behaviour. Animal Behaviour 28:752–762.

Brown, J. H., J. F. Gillooly, A. P. Allen, V. M. Savage, and G. B. West. 2004. Toward a metabolic theory of ecology. Ecology 85:1771–1789.

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Dell, A. I., S. Pawar, and V. M. Savage. 2013. Temperature dependence of trophic interactions are driven by asymmetry of species responses and foraging strategy. Journal of Animal Ecology. In press.

Englund, G., G. Ohlund, C. Hein, and S. Diehl. 2011. Temperature dependence of the functional response. Ecology Letters 14:914–921.

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