Examining Bergmann's rule in a cosmopolitan marine mammal, the bottlenose dolphin (Tursiops spp.)

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Abstract

Body size is a life-history trait with significant ecological and physiological implications. As a group, marine mammals are the largest mammals on earth. The smallest marine mammal (by mass) is the marine otter (Lontra felina), weighing 3–5 kg (Jefferson et al., 2015), which is over 10 times as much as the smallest terrestrial mammal, the Etruscan shrew (Suncus etruscus), weighing 1.8 g (Jürgens, 2002). Similarly, for the opposite end of the size spectrum, the blue whale (Balaenoptera musculus)—the largest animal to have ever lived—is approximately 150,000 kg (Sears & Calambokidis, 2002) compared to the 5,000 kg African elephant (Loxodonta africana; Laurson & Bekoff, 1978). The large body size attained by marine mammals represents an evolutionary trend to balance energy costs associated with thermoregulation and foraging (Gearty et al., 2018; Goldbogen, 2018; Williams, 1999) and selects for larger neonates (Christiansen et al., 2014, 2018). The lower limit of body size in marine mammals is thought to be constrained by the thermal demand of seawater, which conducts heat 25 times faster than air at the same temperature. Body size largely determines surface area to volume (SA:V) ratios. Smaller animals have a larger surface area for a given volume, resulting in thermoregulatory consequences. Surface area (SA) represents the area over which heat can be lost to the environment. Volume (V) represents internal heat generation as metabolism scales with mass, which scales isometrically with volume. Large body size is advantageous for conserving heat since larger animals have lower SA:V ratios due to the scaling relationships between length, SA (length2), and V (length3) (reviewed by Ashton et al., 2000). This scaling relationship yields a more rapid increase in V than in SA with body length (cubed vs. squared), resulting in greater heat generation and retention relative to heat dissipation. In marine mammals, species inhabiting colder climates minimize their SA:V ratio by changing body shape and/or increasing body size, which reduces heat loss compared to those in warmer climates (Adamczak et al., 2020; Worthy & Edwards, 1990). This trend has been described for both terrestrial (James, 1970) and marine mammals (Ashton et al., 2000; Torres-Romero et al., 2016) under Bergmann's rule. Bergmann's rule was first proposed in 1847 (Bergmann, 1847) to explain the congeneric pattern of larger animals (specifically endotherms) in higher latitudes with colder climates. Since its conception, Bergmann's rule has also been investigated within species and across species as well as in endotherms and ectotherms, demonstrating its open criteria (Meiri, 2011). In marine species, Bergmann's rule is supported on a broad taxonomic level across pinnipeds and cetaceans (Torres-Romero et al., 2016) and within genera for pilot whales (Globicephala spp.) in the North Atlantic (Adamczak et al., 2020). Here we investigate Bergmann's rule in bottlenose dolphins (Tursiops spp.); we specifically examined how body size and resulting relationships between SA and V vary relative to thermal habitat. This cosmopolitan marine mammal ranges widely from tropical to temperate waters (Wells & Scott, 2018). Few small cetaceans span such a broad geographic and thermal range as the bottlenose dolphin, which allows for a unique examination of relationships between thermal habitat and body size of a marine mammal. We obtained morphometric and life history data from 1,035 dolphins from the genus Tursiops spanning a wide geographic and temperature range: T. truncatus and T. erebennus from the North Atlantic (including the Gulf of Mexico, hereafter referred to as North Atlantic) and North Pacific Oceans and T. aduncus from the Indian and Pacific Oceans (Costa et al., 2022a; Hale et al., 2000; Wang, 2018; Wells & Scott, 2018). The focus of this study is on the North Atlantic dolphins, which comprised 92% of the final data set consisting of 229 individuals (see below for selection criteria used). Due to the small sample outside of the North Atlantic, the North Pacific and Indo-Pacific dolphins were included as comparative case studies to avoid confounding factors related to different oceanography that may blur the patterns and challenge our ability to make inferences about Bergmann's rule. Data were obtained from long-term resident wild dolphins in Florida during catch-and-release health assessments, from dolphins taken incidental to fishing operations, and from strandings, in collaboration with several stranding response programs and institutions (Table 1). Dolphins were categorized into the following seven groups (hereafter referred to as populations) based on geographic and thermal habitat, morphotype, and the National Marine Fisheries Service Marine Mammal Stock Assessment Reports (Hayes et al., 2019, 2021, 2023): Sarasota Bay, coastal mid-Atlantic, offshore mid-Atlantic, offshore NW Atlantic, NE Atlantic, California, and Shark Bay (Table 1). SA and V were calculated using two symmetrical cones to compare how body size differs among these different populations (Figure 1). A comparison of this simple geometric model to a cast of an adult bottlenose dolphin carcass (244 cm female from the mid-Atlantic) revealed the geometric model underestimates surface area by ~10% (cast surface area = 18,900.71 cm2; geometric model surface area = 17,106.65 cm2); however, it was the most parsimonious method (adapted from the truncated cones methods; Gales & Burton, 1987) given the common measurements available across the data sets. We included individuals with girth measurements either immediately anterior to the dorsal fin or midway from the axilla to the dorsal fin, representing maximum girths. We compared the measurements of individuals with both available and failed to find a significant difference (Figure S1; n = 23, V = 72, p = .57, Wilcoxon signed-rank test; Woolson, 1998). Individuals were excluded if they lacked a straight body length measurement (i.e., measured from the tip of the rostrum to the fluke notch), had developmental issues that limited their size, or had girth measurements that were likely greater than normal due to pregnancy or bloating from decomposition at the time of measurement. We also checked for outliers in the girth data and SA:V data and excluded individuals that were beyond 1.5 times the interquartile range in either direction (i.e., Q1–1.5 × IQR or Q3 + 1.5 × IQR). These exclusion criteria were selected so that the data best represented nonpregnant individuals in good body condition while retaining as large a sample size as possible given the difficulty of accessing stranded dolphins in remote locations (e.g., Shark Bay). Analyses included only adult or mature bottlenose dolphins as indicated by a life history class category or age. Dolphins measured during catch-and-release health assessments in Sarasota Bay, Florida, were considered physically mature if their age was at least 10 or 15 years for females and males, respectively, based on visual assessment of the Gompertz growth model in Read et al. (1993). Because longitudinal measurements were available for some Sarasota Bay dolphins across their life, we randomly selected one sampling period for each individual adult with repeat measurements. This was done by a random draw for each individual with repeat measurements with an equal probability of selection. Due to the large sample size (284 total measurements from 126 unique adult individuals), the randomization process for selecting nonrepeat measurements used in the analysis did not affect the results. For individuals where life history class was not provided, we determined a sex-specific minimum adult size (using length measurements) for each population based on the data available and assigned dolphins to the adult category if they were greater than this sex- and population-specific minimum threshold (Table 2). The remaining individuals of unknown life history class or sex were excluded. The population- and sex-specific sample sizes provided in Table 2. Body length and SA:V ratio of adult dolphins were compared among populations using the Kruskal-Wallis rank sum test, and if these respective tests indicated differences, pairwise comparisons were performed using Dunn's test (Dunn, 1964). Nonparametric tests were used because they are more robust to deviations from normality (as observed in Figure S2) when the sample size is limited (Kitchen, 2009). We fit nonlinear regressions to the SA and V data of all Atlantic Ocean dolphins (SA = constant × Vexponent) using nonlinear least squares approximation and compared the nonlinear coefficient (exponent) to the expected geometric scaling relationship (SA = constant × V2/3). We also performed standardized major axis (SMA) regressions on the log-transformed data using the “smatr” package in R (Warton et al., 2012) to compare the relationships between SA and V among populations and to the expected geometric scaling relationship. All statistical tests were performed in R (R Core Team, 2023), and a p value of .05 was used to determine the significance of all tests. The data were also visually inspected to corroborate the statistical results and determine if differences existed. All values are reported as the mean ± standard deviation unless otherwise specified. To test whether Bergmann's rule is followed by these bottlenose dolphin populations, average monthly sea surface water temperature (at 0.5 m depth; the shallowest depth available representing the surface) was obtained for the years 1993–2020 from the E.U. Copernicus Marine Service Information (data product GLOBAL_MULTIYEAR_ PHY_001_030, downloaded December 2023). These years span most of the dates when the dolphins were sampled and were the complete years available in this data product at time of download. Surface temperatures were extracted for point locations chosen at the center of each bay or mid-latitude across the range to provide a representative time series of average monthly temperatures: Sarasota Bay (27.3°N, 82.5°W), coastal mid-Atlantic (34.0°N, 77.5°W), offshore mid-Atlantic (34.0°N, 73.5°W), offshore NW Atlantic (40.0°N, 71.3°W), NE Atlantic (58.5°N, 1.8°W), California (34.3°N, 121.0°W), and Shark Bay (25.5°S, 113.3°E). We averaged monthly averages across years to depict seasonal fluctuations in sea surface water temperature (Figure 2). We ran two generalized linear regression models—one for length and one for SA:V—using a Gamma family with identity-link function to test whether water temperature is an important predictor of body size. We included sex as a fixed factor because we found male and female dolphins to be different in body size for three of the populations (Figure S2). To account for these sex differences, we repeated our pairwise comparisons of length and SA:V between populations using only male or only female dolphins (Figure S3). We report patterns that are consistent across analyses (male only, female only, and both sexes). Adult bottlenose dolphins in the Atlantic Ocean show increasing body size as the population's latitude increases (Figure 3). Both length and SA:V are statistically different across these populations (length: χ2 = 118, df = 4, p ≪ .0001, SA:V: χ2 = 103, df = 4, p ≪ .0001), and pairwise comparisons shown in Figure 3 indicate which populations are different. Both NE Atlantic and offshore NW Atlantic dolphins are significantly larger than Sarasota Bay bottlenose dolphins (Figure 3). The larger dolphins (NE Atlantic and offshore NW Atlantic) experience colder waters with average monthly temperatures <15°C for at least half of the year, while the average monthly temperature in Sarasota Bay remains above 15°C (Figure 2). Offshore dolphins (mid-Atlantic and NW Atlantic populations) experience much higher maximum temperatures; yet, we found no statistical difference in length or SA:V ratio between these populations and NE Atlantic dolphins (Figure 3). When considering the case study of Shark Bay dolphins, the data suggest they are shorter than other populations and thus have larger SA:V ratio (Figure 3, Table 3). Although water temperatures in Shark Bay were comparable to those in Sarasota Bay and the mid-Atlantic (coastal and offshore), the range of average monthly water temperatures across the year is much smaller for Shark Bay (5°C compared to 8°C–13°C), resulting in a warmer thermal regime year-round (Figure 2). As a contrasting case study example, the California dolphins appear to be similar in length and SA:V ratio to the Atlantic dolphins inhabiting more northerly latitudes (i.e., offshore mid-Atlantic, offshore NW Atlantic, and NE Atlantic). However, the thermal regime of California dolphins was colder than that of the offshore mid-Atlantic dolphins, warmer than that of the NE Atlantic dolphins, and spanned a small range of the offshore NW Atlantic dolphins' thermal regime (Figure 2, Table 3). That California dolphins appear to be similarly sized to these Atlantic dolphin populations while experiencing a different thermal regime may indicate that in disparate ocean basins there are alternative drivers of body size that extend beyond temperature. Other factors may include the abundance and predictability of prey and its interaction with diving ability (i.e., larger animals can dive longer and reach deeper prey; Costa & Favilla, 2023). When we examined the relationship between body size for a population (length or SA:V) and water temperature (mean, minimum, maximum, and range) using generalized linear models with sex as a fixed factor, both sex and temperature were highly significant (p ≪ .0001) in all the models regardless of which temperature metric was used. Using the corrected Akaike information criterion, we found that SA:V was best predicted by the model with mean temperature while length was best predicted by the model with maximum temperature (Figure 4, Table S1). Both models had similarly high adjusted values and for models SA:V and length, a large of the in body size is by the temperature metric when sex is SA V the nonlinear of their SA:V relationship (Figure We found that the SA:V relationship to the of which significantly from the expected scaling of (Figure the SA:V relationship among populations is and surface area increases more than expected a given in volume. When the ranges that populations this we found that NE Atlantic dolphins had the largest range in both SA and as well as the mean SA and large body size is likely to their however, the high of in body size is given the seasonal in temperature. The Sarasota Bay dolphins were some of the smallest in SA and V of the Atlantic dolphins, their SA and V ranges with most or all of the respective ranges of the mid-Atlantic dolphins (coastal and The case study Shark Bay dolphins the range of SA and V on the from the other A comparison of the relationship between SA and V among populations using regression on a the Atlantic Ocean populations have that significantly among populations = df = 4, p = from to (Table S2). The for all Atlantic dolphins other than the offshore NW Atlantic population was significantly lower than the expected of (Figure Table S2). to the offshore NW Atlantic the Shark Bay and California populations have that did not significantly from the expected The patterns suggest that bottlenose dolphins Bergmann's rule as the largest dolphins are found in the waters and the smallest dolphins are in the least water Both NE Atlantic and offshore NW Atlantic dolphins experience the temperatures at the latitudes and are the largest As the population of smallest dolphins, Shark Bay dolphins have a larger SA relative to size across which to small size may be due to the thermal of in Although the mean and maximum water temperature are higher in Sarasota Bay than in Shark Bay, the seasonal in water temperatures in Florida is greater with colder water in the (Figure 2). This that the minimum water temperature and/or the seasonal temperature may the lower limit in Sarasota Bay dolphins to colder However, minimum water temperature and temperature range were not the best for the body size that other than (i.e., or may be more important for with large seasonal temperature (Adamczak et al., et al., et al., This is supported by the offshore mid-Atlantic dolphins and offshore NW Atlantic dolphins, which experience different temperature ranges and are not significantly different in size (Figure 3). Both populations of offshore dolphins are also not statistically smaller than NE Atlantic dolphins, experiencing warmer waters either Atlantic) or year-round at lower latitudes that may to their similarly large size different thermal are the offshore and associated with such as at and larger (Costa & Favilla, & 1990). studies have found differences between coastal and offshore bottlenose dolphins in the same that extend beyond size & 1990). In to smaller body coastal bottlenose dolphins have longer and compared to offshore dolphins et al., & which may as a thermal to heat or provide greater for their prey or data from that warmer water dolphins are longer and more while colder water dolphins are more in body size in in However, these from both temperature and prey factors that are to since colder waters are more than warmer waters & it is important to how habitat and also body size and (Costa & Favilla, & 1990). data were limited by disparate sample sizes across populations and included a small of bottlenose dolphin populations and species within the genus However, the North Atlantic populations a range of latitude and thermal which is the for Bergmann's rule. standard measurements body length and maximum were available across populations in our which to also SA:V important morphometric factor that an thermal morphometric measurements (e.g., girth at the and of how differs among the populations (e.g., relative our analyses using length and SA:V ratio revealed body in bottlenose dolphins that Bergmann's with dolphins inhabiting colder climates than their an body in has been described with smaller dolphins at higher latitudes and increasing body size with colder temperatures & et al., Shark Bay dolphins in were included in these and are a different species than North Atlantic dolphins truncatus and T. & the on the relationships among in the genus is et al., Costa et al., et al., 2020). We included Shark Bay dolphins to the smallest species in the genus that a unique thermal environment. small size may from the thermal of their habitat where consistent year-round temperatures and a habitat depth of et al., with dolphins of the provide from A habitat also their small size as has been proposed for the sea Costa & Favilla, et al., waters have (i.e., et al., Shark Bay et al., 2011). analyses revealed dolphins in the bay on the or than the et al., Similarly, California dolphins provide an of population outside of the North Atlantic Ocean that a similarly much colder thermal regime in a by coastal et al., These populations the to this study with more populations (i.e., from different and from the to Bergmann's rule at a and at (e.g., Torres-Romero et al. studies focus on body length or as the body size metric which to Bergmann's rule (Ashton et al., 2000; Torres-Romero et al., SA:V ratio has greater to heat which to a relationship with temperature than body To the thermoregulatory of body size and thus SA:V in Bergmann's rule in marine mammals, and as well as their seasonal also be considered in analyses when possible & et al., in water temperature can foraging and thus energy & et al., 2011). and determine its which heat from the to its thus heat et al., et al., et al., However, of the and thermal and can this when et al., et al., examination of and relative to size and metabolism on a seasonal provide into the drivers and at a than the evolutionary of Bergmann's rule. body size is by physiological and ecological beyond Body size dive limit and diving et al., energy et al., 2020; et al., Williams, and and et al., et al., individuals have a greater dive to dive deeper and which be advantageous for prey at depth et al., The and size of prey energy and the ability to larger et al., Smaller individuals can on lower energy and thus in (Costa & Favilla, 2023). the other larger individuals can longer due to their energy & 2018). This energy has thermoregulatory as the of marine mammals also as a thermal As are associated with body size, and energy larger marine mammals have higher and can provide more to (Costa & higher and This relationship has been most in pinnipeds et al., et al., et al., and high have also been in NE Atlantic dolphins inhabiting et al., These of large size body size between evolutionary and the thermoregulatory of SA:V Although to body size, and in may to individuals a range of thermal there are related to body size, and temperature is only one of of the smallest the how these other factors may to Bergmann's rule. have and and high which to internal heat and a large to in water et al., et al., et al., 2018). such high and high which can have several ecological et al., the opposite end of the size spectrum, the largest cetaceans are of which have geographic ranges due to their For example, blue whales (Balaenoptera from to tropical to and to et al., 2018; et al., The large body size of in to their a life history of heat than heat retention & likely the relationship between body size and temperature. Torres-Romero et al. found that than was a predictor of body size for with this examination of thermal and body was to into the ecological and factors in body size in cetaceans and the temperature in these measurements on cetaceans are to thus the of using stranded individuals and morphometric data across programs (e.g., et al., 2016) to to and body size on a We to the and the data used in this analysis from stranded and dolphins over years the following the Sarasota Marine in the of North the Marine of the of the Shark Bay National Marine Fisheries Service Fisheries the the and Marine the the in and the of Marine mammal stranding response in the was under the Marine Mammal or National Marine Fisheries Service and under and in by The data over were provided the of and Scott, in to and for data in Sarasota Bay has from National Marine Fisheries and the of among Data from Sarasota Bay were a series of National Marine Fisheries Service and Marine Data from Shark Bay were supported by National to We to the for their that this and and data and Data and Data and Data and Data and Data and T. Data and Data and Data and and Information The is not for the or of information by the than be to the for the

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