DOI: 10.5061/dryad.zcrjdfnhf
title: Size-associated energetic constraints on the seasonal onset of reproduction in a species with indeterminate growth

description: The seasonal onset of reproduction is constrained in many systems by a
 need to first accumulate energetic reserves. Consequently, the observation
 that larger individuals reproduce earlier may be due to a negative
 relationship between size and mass-specific basal metabolic rate that is
 shared across diverse taxa. However, an untested prediction of this
 hypothesis is that individuals should be metabolically efficient enough to
 escape energetic constraints above a certain size threshold. Seasonally
 reproducing species, such as temperate fishes, that must recover winter
 energy losses before reproduction and exhibit indeterminate growth are
 ideal models to test this prediction. We harness decade-long behavioral
 data on parental male smallmouth bass, Micropterus dolomieu, to
 investigate contributions of energetic allometry to differences in
 reproductive timing. At the population level, peak seasonal reproductive
 timing (i.e., the median date on which eggs were found in nests each year)
 was negatively related to degree days–a measure of thermal energy
 experienced–before reproduction. At the individual level, degree days
 accumulated by males before reproduction was related to male size and
 condition in every year, but the impact of temperature on reproductive
 timing by the largest males was relaxed in most years. Additionally, we
 used our data to replicate the analyses of two previous studies of M.
 dolomieu populations and found virtually identical negative associations
 between male body size and degree days accumulated before reproduction.
 Our results suggest that in smallmouth bass the onset of seasonal
 reproduction is constrained by basal metabolic rate–as indicated by total
 length–and that large individuals can escape size-associated energetic
 constraints. We reveal a more complicated relationship between size and
 reproductive timing than earlier studies, which may be relevant for many
 species. Knowledge of this relationship is critical to understanding how a
 changing climate will influence population dynamics of economically,
 ecologically, and recreationally important species like M. dolomieu.
description: <strong>Study
 site</strong> We conducted this study in 1999 and 2001–2009 on
 Pallette Lake, a 70-ha research lake in the Northern Highlands Fishery
 Research Area of north-central Wisconsin (46.067° N/89.604° W). The Wisconsin Department of Natural
 Resources manages this lake, which is closed to fish migration and has a
 maximum depth of approximately 20 m and a mean depth of approximately 10
 m. Saunders et al. (2002) describe the benthic and limnological
 characteristics of the lake in detail. Anglers are subject to a mandatory
 creel census, where caught fish must be reported to ensure regulations are
 followed. From 1999–2006, regulations required anglers to return to the
 lake any male less than 41 cm total length and from 2007 onwards all males
 under 51 cm had to be returned. We had significant representation of males
 larger than 40 cm in our analyses (13.8%).  
 <strong>Annual nest
 census</strong> We initiated surveys each year when the water
 temperature approached 15 °C,
 typically in mid to late May, and continued until males ceased nest
 construction (late June to early July) and progeny in most nests had
 dispersed. Two to three crew members with snorkels searched for nests as
 they swam transects running from the shoreline out to a depth of about 4
 m. This depth was well beyond both the average 1.7 m depth at which nests
 in the lake were found and the maximum depth of smallmouth bass nests
 found in studies of other Wisconsin lakes (Bozek et al. 2002). When each
 nest was discovered, snorkelers placed a numbered tag constructed from a
 strip of Rite-n-Rain paper tied to a sinker on the edge of the nest and
 recorded the date, stage of embryos (if present), depth, location and
 distinctive landmarks that might be useful to relocate
 nests. <strong>Characteristics of parental
 males</strong> We captured parental males from their nests with
 hand nets and recorded their total length (cm) and weight (g). Each male
 was marked with a uniquely numbered Floy FD-67C anchor tag
 (University of Wisconsin RARC protocol
 A-48-9700-L00173-2-04-99). These tags
 allowed us to track individuals across seasons and estimate the total
 number of males that spawned each year, although analyses on reproductive
 timing were limited to those males that were found with eggs in their nest
 to ensure estimates of degree days before reproduction were comparable
 across individuals (Table 1).
 <strong>Temperature and
 degree days</strong> We used temperature data to estimate the thermal
 energy experienced by males in each year. A thermograph positioned near
 the shoreline at an approximate depth of 1 m recorded the water
 temperature (°C) hourly when the lake was not covered by ice. Thermograph
 malfunctions or other disturbances (e.g., removal of the thermograph from
 the lake by a lake visitor) resulted in some missing temperature records
 over the 10 years. We estimated these records using regression equations
 that characterized the relationship between water temperature in our study
 site (Pallette Lake) and nearby Sparkling Lake (46.010° N/89.701° W), a
 North Temperate Lakes Long-Term Ecological Research lake (64 ha; maximum
 depth 20 m) that has a nearly identical temperature profile as Pallette
 Lake (range of adjusted <em>R<sup>2</sup></em>
 over the 10-year study: 0.87–0.99; <em>P</em> &lt; 0.0001;
 Supplementary Figure S1 and Table S1).
 These temperature data were used
 to compute degree days, a measure of the thermal energy experienced by
 individuals (Chezik et al.
 2014a, b).  In particular, we used the sum of positive differences between
 the average daily water temperature at 1 m and the threshold
 T<sub>0</sub> = 10 °C for each day until the date that the
 average water temperature reached 15 ºC, the temperature at which seasonal
 reproductive activity is typically initiated, to evaluate the
 population-level reproduction response to temperature each year (Shuter et
 al. 1980; Ridgway et al. 1991; Lukas and Orth 1995). The sum of degree
 days each year from the first date on which the water temperature was
 favorable for energy recuperation (i.e., average exceeded 10 °C) until the
 date at which eggs were found in the nest of a male was also computed to
 produce a measure of the seasonal thermal energy experienced by each
 parental male prior to reproduction and evaluate individual responses to
 temperature (Shuter et al. 1980; Ridgway et al. 1991). In addition, we
 calculated the average and maximum temperature of the growth season for
 every year, defined as the period between the first day the average
 temperature climbed above 10 ºC and the last day before the average
 temperature dropped below 10 ºC, and the duration of winter, defined as
 the number of days between growth seasons (Shuter et al., 1980; Ridgway et
 al., 1991; Table 1). These latter measures of thermal energy were used to
 explore how temperature may control a size threshold at which males are
 released from energetic constraints on seasonal reproductive
 phenology. <strong>Statistical
 analyses</strong> <em>Estimating body
 condition</em> Individual condition, often measured as some
 function of body mass, may provide an estimate of energetic reserves for
 individuals of a specified size and, hence, influence reproductive
 phenology (Kaufman et al. 2007, Schloesser and Fabrizio 2017). Individual
 condition was calculated as the residual of the relationship between
 weight (natural log [ln] transformed) and length (ln transformed) for each
 year, which has been shown to successfully predict energy content in a
 broad set of fish species (Kaufman et al. 2007, Schloesser and Fabrizio
 2017). <em>Population-level responses to thermal energy</em>
 We used linear regression to
 predict annual population response times, the time interval between the
 date on which the mean water temperature reached 15 ºC and the median date
 on which eggs were found in nests, from the number of degree days
 accumulated before the first 15 ºC day each year.  If
 thermal
 energy controls individual
 reproductive readiness, then we expect the slope of this relationship to
 be negative (Shuter et al. 1980).
 <em>Individual behavioral
 response to thermal
 energy</em> We first used a linear mixed model structured
 similarly to those used in prior studies on smallmouth bass reproductive
 timing, where size was regressed on reproductive timing and year, to
 generate a comparable measure of the relationship between male total
 length (ln transformed) and the number of degree days (ln transformed,
 threshold T<sub>0</sub> = 10 °C) that had
 accumulated up to the date on which a male spawned (i.e., the date a nest
 was found to contain eggs) (Ridgway et al. 1991; Lukas and Orth, 1995).
 Individual identifiers were included as a random effect because 316
 individuals bred in more than one season. If a temperature-dependent
 metabolic process is the main driver of reproductive timing,
 species-specific constants in allometric scaling laws predict the slopes
 of these relationships to be similar across studies (West et al.
 1997).  Next, to examine predictions related to the
 presence of an energetic threshold and to explore whether incorporating
 condition improves predictions of reproductive timing, we fit and competed
 a set of models predicting the degree days a male accumulated prior to
 reproduction. Alternative models included as predictors
 all combinations
 of condition, length (ln
 transformed), and length<sup>2</sup> (ln transformed), which
 allowed the effect of body size on reproductive timing to vary. Indicators
 for years and a random effect for individuals were included in all models.
 Models were tested with and without year interactions with condition or
 the two body length terms. Akaike information criterion (AIC) was used to
 choose between models (Akaike 1973). Some males spawned more than once
 within a season (N=127). In these cases, we restricted the analysis to the
 first attempt within a year. We excluded data from approximately one-third
 of males (34.6%) whose nests were discovered after eggs had hatched
 because timing of reproduction could not be definitively determined for
 these males. The mean size and range of sizes of these males were
 qualitatively very similar to those included in the study so we did not
 expect this to bias our results. If larger males experience less severe
 winter energy losses, then the slope of the relationship between male length
 and degree days accumulated before reproduction is expected to be
 negative in each year
 (Ridgway et al. 1991). If there is a size threshold above which males can
 escape energetic constraints on reproduction, we expected the quadratic
 length term to be included in the chosen model. Similar models including
 condition, length (ln transformed), and length<sup>2</sup> (ln
 transformed) as predictors of reproductive timing were conducted for each
 year independently to validate results of our comprehensive model
 (Supplement; Supplementary
 Table S3). Post hoc linear models were conducted to test
 the hypothesis that in years
 where environmental
 conditions favored the accumulation of greater energetic reserves,
 energetic constraints on reproduction should be restricted to smaller
 individuals (Supplementary Table S4). Specifically, we investigated the
 relationship between the size threshold at which there was no relationship
 between size and degree days before reproduction in a given year–given by
 the untransformed body length of the parabolic vertex in the best
 regression models–and environmental variables that we hypothesized might
 influence the size threshold at which individuals are released from
 metabolic constraints (Supplementary Table S4). These environmental
 variables included the degree days accumulated before 15 ºC, the duration
 (days) of the winter, the duration (days) of the previous season, the
 number of degree days accumulated during the previous growth season, and
 the average temperature of the previous growth
 season.
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