Russel D. Andrews

Allometric cascade as a unifying principle of body mass effects on metabolism

The power function of basal metabolic rate scaling is expressed as aMb, where a corresponds to a scaling constant (intercept), M is body mass, and b is the scaling exponent. The 3/4 power law (the best-fit b value for mammals) was developed from Kleibers original analysis and, since then, most workers have searched for a single cause to explain the observed allometry. Here we present a multiple-causes model of allometry, where the exponent b is the sum of the influences of multiple contributors to metabolism and control. The relative strength of each contributor, with its own characteristic exponent value, is determined by the control contribution. To illustrate its use, we apply this model to maximum versus basal metabolic rates to explain the differing scaling behaviour of these two biological states in mammals. The main difference in scaling is that, for the basal metabolic rate, the O2 delivery steps contribute almost nothing to the global b scaling exponent, whereas for the maximum metabolic rate, the O2 delivery steps significantly increase the global b value.

A novel method for identifying behavioural changes in animal movement data

A goal of animal movement analysis is to reveal behavioural mechanisms by which organisms utilize complex and variable environments. Statistical analysis of movement data is complicated by the fact that the data are multidimensional, autocorrelated and often marked by error and irregular measurement intervals or gappiness. Furthermore, movement data reflect behaviours that are themselves heterogeneous. Here, we model movement data as a subsampling of a continuous stochastic processes, and introduce the behavioural change point analysis (BCPA), a likelihood-based method that allows for the identification of significant structural changes. The BCPA is robust to gappiness and measurement error, computationally efficient, easy to implement and reveals structure that is otherwise difficult to discern. We apply the analysis to a GPS movement track of a northern fur seal (Callorhinus ursinus), revealing an unexpectedly complex diurnal behavioural profile, and demonstrate its robustness to the greater errors associated with the ARGOS tracking system. By informing empirical interpretation of movement data, we suggest that the BCPA can eventually motivate the development of mechanistic behavioural models.

First Long-Term Behavioral Records from Cuvier’s Beaked Whales (Ziphius cavirostris) Reveal Record-Breaking Dives

Cuvier’s beaked whales (Ziphius cavirostris) are known as extreme divers, though behavioral data from this difficult-to-study species have been limited. They are also the species most often stranded in association with Mid-Frequency Active (MFA) sonar use, a relationship that remains poorly understood. We used satellite-linked tags to record the diving behavior and locations of eight Ziphius off the Southern California coast for periods up to three months. The effort resulted in 3732 hr of dive data with associated regional movements – the first dataset of its kind for any beaked whale – and included dives to 2992 m depth and lasting 137.5 min, both new mammalian dive records. Deep dives had a group mean depth of 1401 m (s.d. = 137.8, n = 1142) and duration of 67.4 min (s.d. = 6.9). The group mean time between deep dives was 102.3 min (s.d. = 30.8, n = 783). While the previously described stereotypic pattern of deep and shallow dives was apparent, there was considerable inter- and intra-individual variability in most parameters. There was significant diel behavioral variation, including increased time near the surface and decreased shallow diving at night. However, maximum depth and the proportion of time spent on deep dives (presumed foraging), varied little from day to night. Surprisingly, tagged whales were present within an MFA sonar training range for 38% of days locations were received, and though comprehensive records of sonar use during tag deployments were not available, we discuss the effects frequent acoustic disturbance may have had on the observed behaviors. These data better characterize the true behavioral range of this species, and suggest caution should be exercised when drawing conclusions about behavior using short-term datasets.

Three-dimensional resting behaviour of northern elephant seals: drifting like a falling leaf

During their long migrations through the Pacific, northern elephant seals, Mirounga angustirostris, never haul out on land and they rarely spend more than a few minutes at a time at the surface. They are almost constantly making repetitive, deep dives, raising the question of when do they rest? One type of dive, the drift dive, characterized by a time-depth profile with a phase of lower than average descent speed is believed to be a resting dive. To examine the behaviour of seals during drift dives, we measured body position and three-dimensional diving paths of six juvenile seals. We found that seals rolled over and sank on their backs during the drift phase, wobbling periodically so that they resembled a falling leaf. This enabled seals to drastically slow their descent rate, possibly so that negatively buoyant seals can rest without ending up in the abyss. This reduces the work required to return to the surface to breath, and allows them time to rest, process food or possibly sleep during the descent phase of these dives where they are probably less susceptible to predation.

Heart Rate and Oxygen Consumption of Northern Elephant Seals during Diving in the Laboratory

Many techniques have been employed to measure metabolic and cardiovascular changes in diving marine mammals. Each of these methods has its advantages, but the methods also have drawbacks when applied to phocid seals. The aim of this study was to investigate heart rate and metabolic responses to diving in juvenile northern elephant seals that are not associated with forced changes in exercise state, and, secondarily, to investigate whether heart rate could be used as an indicator of metabolic rate in this species. Six seals were allowed to dive freely in a metabolic chamber while simultaneous measurements of heart rate and oxygen consumption were made. Within each dive cycle (dive and surface interval), the seals spent an average of 74% of the time submerged. Mean dive duration was 6.43 ± 0.6 (SD) min. Mean oxygen consumption during diving was 3.32 ± 0.4 mL O2 min−1 kg−1, a decrease of approximately 26% from baseline values. An inverse relationship was observed between oxygen consumption and the percentage of time spent submerged in each dive cycle. The total amount of oxygen consumed during the surface interval increased with increasing dive duration, while the duration of the surface interval itself did not change, indicating that seals alter the rate of O2 uptake rather than the time spent at the surface. Mean heart rate during diving was 34.5 ± 6.2 beats min−1, 36% lower than resting values. Mean diving heart rate was independent of dive duration, percent time submerged, and oxygen consumption. Mean surface interval heart rate was 66.6 ± 11.1 beats min−1and was not correlated with oxygen consumption. Average heart rate over the entire dive cycle increased with increasing oxygen consumption in all of the seals, but there was only a significant relationship in two seals, which casts some doubt on the usefulness of heart rate as an indicator of metabolic rate in this species. While providing important information on the changes in heart rate and oxygen consumption during diving in northern elephant seals, a complete understanding of the diving metabolic rate of these animals will require a combination of approaches that can be used in concert with data on freely living animals.

Predicting metabolic rate from heart rate in juvenile Steller sea lions Eumetopias jubatus.

SUMMARY The validity of using heart rate to estimate energy expenditure in free-ranging Steller sea lions Eumetopias jubatus was investigated by establishing whether there is a relationship between heart rate (fH) and oxygen consumption rate (V̇O2) in captive sea lions while swimming and resting. Four trained Steller sea lions (2 males and 2 females; mass 87.4–194.4 kg; age 16 months–3 years) were each equipped with a datalogger and two dorsal subcutaneous electrodes to record electrocardiograms from which fH was calculated. V̇O2 (measured using open-circuit respirometry) was simultaneously recorded while the previously fasted animals were at rest within an enclosed dry metabolic chamber or while they swam in an enclosed swim mill against water currents of various speeds (0–1.5 m s–1). The mean regression equation describing the relationship between fH (beats min–1) and V̇O2 (ml h–1 kg–0.60) for all four animals was V̇O2 =(71.3fH±4.3)–(1138.5±369.6) (means± S.E.M.) (r2=0.69, P<0.01). The relationship demonstrated between fH and V̇O2 while fasting suggests that heart rate can potentially be used to monitor energy consumption in free-ranging Steller sea lions. However, a short-term feeding experiment revealed no significant increase in heart rate following a 6 kg or 12 kg meal to match the observed increase in rate of oxygen consumption. This suggests that heart rate may not accurately reflect energy consumption during digestion events. Additional research should be conducted to further elucidate how the relationship between heart rate and oxygen consumption is affected by such factors as digestive state, stress and age.

Effects of Diving and Swimming Behavior on Body Temperatures of Pacific Leatherback Turtles in Tropical Seas

Mathematical models and recordings of cloacal temperature suggest that leatherback turtles (Dermochelys coriacea) maintain core body temperature higher than ambient water temperature (TW) while freely swimming at sea. We investigated the thermoregulatory capabilities of free‐ranging leatherbacks and, specifically, the effect that changes in diving patterns and ambient temperatures have on leatherback body temperatures (TB). Data loggers were used to record subcarapace and gastrointestinal tract temperatures (TSC and TGT, respectively), TW, swim speed, dive depth, and dive times of female leatherback turtles during internesting intervals off the coast of Guanacaste, Costa Rica. Mean TSC (28.7°–29.0°C) was significantly higher than mean TW (25.0°–27.5°C). There was a significant positive relationship between TSC and TW and a significant negative correlation between TSC and dive depth and TGT and dive depth. Rapid fluctuations in TGT occurred during the first several days of the internesting interval, which suggests that turtles were ingesting prey or water during this time. Turtles spent 79%–91% of the time at sea swimming at speeds greater than 0.2 m s−1, and the average swim speed was 0.7 ± 0.2 m s−1. Results from this study show that alterations in diving behavior and TW affect TB of leatherback turtles in the tropics. Body temperatures of free‐ranging leatherback turtles correspond well with values for TB predicted by mathematical models for tropical conditions.

Validation of the use of doubly labeled water for estimating metabolic rate in the green turtle (Chelonia mydas L.): a word of caution.

SUMMARY Marine turtles often have extremely high water turnover accompanied by a low field metabolic rate (FMR), a combination that can contraindicate the use of doubly labelled water (DLW). Therefore, we conducted a validation study to assess the suitability of the DLW technique for determining FMR of marine turtles. Six green turtles (22.42±3.13 kg) were injected with DLW and placed in a tank of seawater with a respirometer for continuous monitoring of oxygen consumption (MR) over a 5-day period. Trials were conducted for turtles in both fed and fasted states. Respiratory exchange ratio (RER) was determined in a dry respirometer and used to calculate energy expenditure. For fed and fasted turtles, total body water (TBW) was 66.67±3.37% and 58.70±7.63% of body mass, and water flux rates were 9.57±1.33% and 6.14±0.65% TBW day–1, respectively. Water turnover in fasted turtles was 36% lower than that of fed turtles but MR (from oxygen consumption) of fasted turtles (13.77±1.49 kJ kg–1 day–1) was 52% lower than in fed turtles (28.66±5.31 kJ kg–1 day–1). Deuterium to oxygen-18 turnover rate (kd:ko) ratios averaged 0.91±0.02 for fed turtles and 1.07±0.16 for fasted turtles. Fed turtles had a mean group difference of 8% and a mean individual difference of 53% between DLW and respirometry. The DLW method gave negative MR values in fasted turtles and could not be compared with respirometry data. Researchers should use caution when applying the DLW method in marine reptiles, especially when high water flux causes >90% of the labeled oxygen turnover to be due to water exchange.

Acidic deposition as an unlikely cause for amphibian population declines in the Sierra Nevada, California

Abstract The Sierra Nevada of California is one of many regions worldwide that has recently experienced dramatic declines in amphibian populations. During the past two to three decades many populations of at least two species ( Rana muscosa and Bufo canorus ) have disappeared in national parks and designated wilderness areas at high elevation, whereas populations of a third widespread species ( Pseudacris regilla ) have remained stable or declined to a lesser extent. Acidification from atmospheric deposition has been suggested as a cause for these disappearances primarily because most surface waters in these areas are exceptionally low in acid neutralizing capacity (ANC), and thus are vulnerable to changes in water chemistry due to acidic deposition. We tested the hypothesis that acidification of habitats has adversely affected amphibian populations by eliminating populations from waters most vulnerable to acidification, i.e. low in pH or ANC, or from waters low in ionic strength, a condition that increases the sensitivity of amphibians to low pH. A survey of 235 potential breeding sites in 30 randomly selected survey areas failed to reveal significant differences in water chemistry parameters between sites with and sites without each of the three species. Moreover, the water chemistry parameters did not differ among sites inhabited by the three species in a manner paralleling their degrees of acid tolerance. These findings contra-indicate acidic deposition as a cause of recent amphibian population declines in the Sierra Nevada at high elevation.

Breathing frequencies of northern elephant seals at sea and on land revealed by heart rate spectral analysis

Elephant seals breathe episodically at sea and on land and surprisingly long apnoeas occur in both situations. An important difference is that recovery from apnoeic periods is much quicker at sea, which might be due, in part, to differences in the ventilatory response. Respiratory frequencies of juvenile northern elephant seals diving at sea and resting on land were estimated from time-frequency maps of the Wigner distribution of heart rate variability. Simultaneous direct measurement of respiration and estimation of respiratory frequency (fR) in the laboratory demonstrated that the error of estimation was small (mean +/- S.D.= 1.05+/-1.23%) and was independent of the magnitude of fR. Eupnoeic fR at sea was 2.4 times higher than on land (22.0+/-2.0 vs. 9.2+/-1.3 breaths min(-1), respectively), facilitating quick recovery from the preceding dive and allowing a 34% increase in time spent apnoeic at sea versus on land. The overall fR (no. of breaths in a eupnoea divided by the total time of the apnoea+eupnoea cycle) of 2.3+/-0.6 breaths min(-1) at sea was no different from the rate on land and was inversely related to the preceding dive duration, suggesting that metabolism on longer dives may be reduced.