Terrie M Williams

University of California, Santa Cruz | UCSC · Department of Molecular Cell & Developmental Biology

Limited polar geographical range, narrowly defined migratory routes, and deep‐diving behaviors make narwhals exceptionally vulnerable to anthropogenic disturbances including oceanic noise. Although behavioral studies indicate marked responses of cetaceans to disturbance, the link between fear reactions and possible injury from noise exposure is lim...

Despite rapid advances in sensor development and technological miniaturization, it remains challenging to non-invasively record small-amplitude electrophysiological signals from an animal in its natural environment. Many advances in ecophysiology and biologging have arisen through sleep studies, which rely on detecting small signals over multiple d...

Background Environmental conditions can influence animal movements, determining when and how much animals move. Yet few studies have quantified how abiotic environmental factors (e.g., ambient temperature, snow depth, precipitation) may affect the activity patterns and metabolic demands of wide-ranging large predators. We demonstrate the utility of...

When navigating heterogeneous landscapes, large carnivores must balance trade‐offs between multiple goals, including minimizing energetic expenditure, maintaining access to hunting opportunities, and avoiding potential risk from humans. The relative importance of these goals in driving carnivore movement likely changes across temporal scales, but o...

One of the last pristine marine soundscapes, the Arctic, is exposed to increasing anthropogenic activities due to climate-induced decrease in sea ice coverage. In this study, we combined movement and behavioral data from animal-borne tags in a controlled sound exposure study to describe the reactions of narwhals, Monodon monoceros , to airgun pulse...

Unlike the majority of marine mammal species, Hawaiian monk seals (Neomonachus schauinslandi) and West Indian manatees (Trichechus manatus latirostris) reside exclusively in tropical or subtropical waters. Although potentially providing an energetic benefit through reduced maintenance and thermal costs, little is known about the cascading effects t...

Sequential diving by wild marine mammals results in a lifetime of rapid physiological transitions between lung collapse-reinflation, bradycardia-tachycardia, vasoconstriction-vasodilation, and oxygen store depletion-restoration. The result is a cycle of normoxia and hypoxia in which blood oxygen partial pressures can decline to <20–30 mmHg during a...

Deep diving air-breathing species by necessity must balance submergence time and level of exercise during breath-holding: a low activity level preserves oxygen stores and allows longer duration submergence whereas high activity levels consume oxygen quickly and shorten submergence time. In this study, we combined high-resolution multi sensor animal...

1. Global biotic and abiotic threats, particularly from pervasive human activities, are progressively pushing large, apex carnivorous mammals into the functional role of mesopredator. Hunters are now becoming the hunted. Despite marked impacts on these animals and the ecosystems in which they live, little is known about the physiological repercussi...

Northern elephant seals (NES, Mirounga angustirostris) undergo an annual molt during which they spend ∼40 days fasting on land with reduced activity and lose approximately one-quarter of their body mass. Reduced activity and muscle load in stereotypic terrestrial mammalian models results in decreased muscle mass and capacity for force production an...

Background: Under current scenarios of climate change and habitat loss, many wild animals, especially large predators, are moving into novel energetically challenging environments. Consequently, changes in terrain associated with such moves may heighten energetic costs and effect the decline of populations in new localities. Methods: To examine...

The narwhal (Monodon monoceros ) is a high‐Arctic species inhabiting areas that are experiencing increases in sea temperatures, which together with reduction in sea ice are expected to modify the niches of several Arctic marine apex predators. The Scoresby Sound fjord complex in East Greenland is the summer residence for an isolated population of n...

Dolphin skin has long been an inspiration for research on drag reduction mechanisms due to the presence of skin ridges that could reduce fluid resistance. We gathered in vivo three-dimensional surface data on the skin from five species of odontocetes to quantitatively examine skin texture, including the presence and size of ridges. We used these da...

Measures of energy expenditure can be used to inform animal conservation and management, but methods for measuring the energy expenditure of free‐ranging animals have a variety of limitations. Advancements in biologging technologies have enabled the use of dynamic body acceleration derived from accelerometers as a proxy for energy expenditure. Alth...

Co‐occurrence with humans presents substantial risks for large carnivores, yet human‐dominated landscapes are increasingly crucial to carnivore conservation as human land use continues to encroach on wildlife habitat. Flexibility in large carnivore behavior may be a primary factor mediating coexistence with people, allowing carnivores to calibrate...

When predators are removed or suppressed for generations, prey populations tend to increase and when predators are re-introduced, prey densities should fall back to pre-control levels. In cases of apparent competition where there are alternate abundant and rare prey species, rare species may decline further than expected or disappear altogether. Re...

Hourly movement data. Hourly movement data for African lions, Grevy’s zebras and Plains zebras used in simulations of encounter rates. (XLSX)

Comparison of ecological conditions. The compatibility of temporally disconnected movement data. (DOCX)

Details of lion collar operation. Dates that collars were operational, number of sample days, hourly distance traveled (SD), and daily distance traveled (SD) for female lions, Plains zebra and Grevy's zebra. Lions with numbers were recaptured more than once and collar either changed or repaired during study. (DOCX)

Ursids are the largest mammals to retain a plantigrade posture. This primitive posture has been proposed to result in reduced locomotor speed and economy relative to digitigrade and unguligrade species, particularly at high speeds. Previous energetics research on polar bears (Ursus maritimus) found locomotor costs were more than double predictions...

Estimation of force generated by dolphins has long been debated. The problem was that indirect estimates of force production for dolphins resulted in low values that could not be validated. Bubble digital particle image velocimetry (DPIV) measured hydrodynamic force production for swimming dolphins and demonstrated high force production. To validat...

A demanding lifestyle Polar bears appear to be well adapted to the extreme conditions of their Arctic habitat. Pagano et al. , however, show that the energy balance in this harsh environment is narrower than we might expect (see the Perspective by Whiteman). They monitored the behavior and metabolic rates of nine free-ranging polar bears over 2 yea...

The mechanism by which odontocetes produce sound is unique among mammals. To gain insight into the physiological properties that support sound production in toothed whales, we examined myoglobin content ([Mb]), non-bicarbonate buffering capacity (β), fiber-type profiles, and myosin heavy chain expression of vocal musculature in two odontocetes: the...

The flight of the narwhal Animals tend to respond to threats with the well-known behaviors of fight, flee, or freeze, each of which requires a different suite of physiological responses. Marine mammals face particular challenges because they may flee into an environment where oxygen is not available and pressure must be accommodated. Williams et al...

Toothed whales use echolocation to sense their environment and capture prey. However, their reliance on acoustic information makes them vulnerable to sound exposure. Odontocetes modify echolocation signals in response to ambient noise levels, yet the metabolic cost of producing and modifying echolocation signals are unknown. Studies on bats found t...

Quantification of fine-scale movement, performance, and energetics of hunting by large carnivores is critical for understanding the physiological underpinnings of trophic interactions. This is particularly challenging for wide-ranging terrestrial canid and felid predators, which can each affect ecosystem structure through distinct hunting modes. To...

Predicted average hourly activity across a 24-hour period for male pumas (±SE) in the Santa Cruz Mountains, CA Arrows correspond to the time of day in which chases for recapture occurred. White arrows show the timing of chases for male puma 36 on Aug. 3, 2015, and black arrows show the timing of chases for male puma 26 on Nov. 18, 2015. Daily activ...

Total number of observed evasive puma behaviors (pooled across all 4 escapes)

Effectiveness of puma 26 M’s figure-of-8 maneuver Trailing distance (m) of hounds rapidly decreased until 9:46:00, when 26 M ran a figure-of-8 pattern and briefly escaped into a tree. This maneuver increased separation distance by nearly 15 m, and the puma’s capture was delayed by an additional 5 min.

Chase 4 reconstruction visualization Video depicts the landscape topography and pursuit dynamics of 4 hounds chasing puma 26 M on the shortest and fastest pursuit of the present study. Map data©2016 Google.

Chase 2 pursuit (red lines = hounds) and escape (blue line = puma) paths and parameters Insets display ODBA (g, B), speed (ms−1, C), and estimated mass-specific metabolic demand (\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{upgreek} \usepackage{...

Chase 3 pursuit (red lines = hounds) and escape (blue line = puma) paths and parameters. Insets display ODBA (g, B), speed (ms−1, C), and estimated mass-specific metabolic demand (\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{upgreek} \usepackage...

Chase 4 pursuit (red lines = hounds) and escape (blue line = puma) paths and parameters Insets display ODBA (g, B), speed (ms−1, C), and estimated mass-specific metabolic demand (\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{upgreek} \usepackage{...

The drive to kill prey is central to understanding the population viability and ecological effects of large carnivores. This drive is modulated by behaviorally determined energetic expenditures, yet current methods of estimating the energetics of terrestrial carnivores are too coarse to inform the fine time scale behavioral decisions that incur the...

Exponential increases in hydrodynamic drag and physical exertion occur when swimmers move quickly through water, and underlie the preference for relatively slow routine speeds by marine mammals regardless of body size. Because of this and the need to balance limited oxygen stores when submerged, flight (escape) responses may be especially challengi...

The broad diversity in morphology and geographic distribution of the 35 free-ranging members of the family Canidae is only rivaled by that of the domesticated dog, Canis lupus familiaris. Considered to be among nature’s most elite endurance athletes, both domestic and wild canids provide a unique opportunity to examine the variability in mammalian...

Tri-axial accelerometers have been used to remotely identify the behaviors of a wide range of taxa. Assigning behaviors to accelerometer data often involves the use of captive animals or surrogate species, as accelerometer signatures are generally assumed to be similar to those of their wild counterparts. However, this has rarely been tested. Valid...

Superimposed on inherently high basal metabolic demands, the additional energetic requirements of reproduction can push female sea otters beyond physiological limits. Indeed, the resulting energy imbalance contributes to disproportionately high rates of mortality at the end of lactation in this species. To examine and quantify metabolic changes ass...

Cetaceans produce different types of sounds that vary according to behavioral context. They also modify their acoustic signals in response to noise. The metabolic costs of producing social sounds and clicks were recently measured in two bottlenose dolphins using flow-through respirometry methods. For both sound types, metabolic rates significantly...

Odontocetes respond to vessels and anthropogenic noise by modifying vocal behavior, surface active behaviors, dive patterns, swim speed, direction of travel, and activity budgets. Exposure scenarios and behavioral responses vary across odontocetes. A literature review was conducted to determine relevant sources of disturbance and associated behavio...

Background The energy requirements of free-ranging marine mammals are challenging to measure due to cryptic and far-ranging feeding habits, but are important to quantify given the potential impacts of high-level predators on ecosystems. Given their large body size and carnivorous lifestyle, we would predict that northern elephant seals (Mirounga an...

The incidence of cardiovascular disease in humans is more than three times that of many wild and domestic mammals despite nearly identical heart morphologies and responses to exercise. A survey of mammalian species from 0.002-kg shrews to 43,000-kg whales shows that the human heart is more dog-like than cat-like and that neither body size nor longe...

Dolphins produce many types of sounds known to have distinct qualities and functionalities. Whistles, which function in social contexts, are much longer in duration and require close to twice the intranasal air pressure to produce relative to biosonar click production. Thus, it is predicted that whistle production would be energetically more costly...

Foraging by large (>25 kg), mammalian carnivores often entails cryptic tactics to surreptitiously locate and overcome highly mobile prey. Many forms of intermittent locomotion from stroke-and-glide maneuvers by marine mammals to sneak-and-pounce behaviors by terrestrial canids, ursids, and felids are involved. While affording proximity to vigilant...

Small body size, large lungs, and dense pelage contribute to the unique challenges faced by diving sea otters (Enhydra lutris) when compared to other marine mammals. Here we determine the consequences of large lungs on the development of diving ability in southern sea otters (Enhydra lutris nereis) by examining the ontogeny of blood, muscle, and lu...

Many animals produce louder, longer or more repetitious vocalizations to compensate for increases in environmental noise. Biological costs of increased vocal effort in response to noise, including energetic costs, remain empirically undefined in many taxa, particularly in marine mammals that rely on sound for fundamental biological functions in inc...

Marine mammals are common, highly visible, and charismatic species that are potentially vulnerable to oil contamination, yet we know surprisingly little about the effects of oil on either individuals or populations. In this regard, the 1989 Exxon Valdez oil spill in the nearshore waters of Alaska is unique. This spill of 11 million gallons of Prudh...

Accelerometers are useful tools for biologists seeking to gain a deeper understanding of the daily behavior of cryptic species. We describe how we used GPS and tri-axial accelerometer (sampling at 64 Hz) collars to monitor behaviors of free-ranging pumas (Puma concolor), which are difficult or impossible to observe in the wild. We attached collars...

Unlike their terrestrial ancestors, marine mammals routinely confront extreme physiological and physical challenges while breath-holding and pursuing prey at depth. To determine how cetaceans and pinnipeds accomplish deep-sea chases, we deployed animal-borne instruments that recorded high-resolution electrocardiograms, behaviour and flipper acceler...

An age-old conflict around a seemingly simple question has resurfaced: why do we conserve nature? Contention around this issue has come and gone many times, but in the past several years we believe that it has reappeared as an increasingly acrimonious debate between, in essence, those who argue that nature should be protected for its own sake (intr...

Pumas (Puma concolor) live in diverse, often rugged, complex habitats. The energy they expend for hunting must account for this complexity but is difficult to measure for this and other large, cryptic carnivores. We developed and deployed a physiological SMART (species movement, acceleration, and radio tracking) collar that used accelerometry to co...

Sea otters (Enhydra lutris) have the highest mass-specific metabolic rate of any marine mammal, which is superimposed on the inherently high costs of reproduction and lactation in adult females. These combined energetic demands have been implicated in the poor body condition and increased mortality of female sea otters nearing the end of lactation...

Widely ranging marine predators often adopt stereotyped, energy-saving behaviours to minimize the energetic cost of transport while maximizing energy gain. Environmental and anthropogenic disturbances can disrupt energy balance by prompting avoidance behaviours that increase transport costs, thereby decreasing foraging efficiency. We examined the a...

Huddling is an important behavior for many endotherms, and it is associated with both social interactions and physiological regulation. Sea lions are highly communal pinnipeds that often congregate in large numbers on coastal rookeries. While this behavior serves a social role, it also has the potential to change the microhabitat and thus the local...

Weddell seals are polar predators that must partition their time between many behaviours, including hunting prey at depth and breathing at the surface. Although they have been well studied, little is known about how foraging behaviour changes when access to breathing holes is restricted, such as in the isolated-hole paradigm. The current study took...

Attempts to measure the propulsive forces produced by swimming dolphins have been limited. Previous uses of computational hydrodynamic models and gliding experiments have provided estimates of thrust production by dolphins, but these were indirect tests that relied on various assumptions. The thrust produced by two actively swimming bottlenose dolp...

Phocids routinely fast for extended periods. During these fasts, energetic requirements are met primarily through the catabolism of blubber lipid. To assess whether fatty acid (FA) composition changes during the postweaning fast in northern elephant seals, blubber biopsies were acquired longitudinally from 43 pups at 2.3 ± 1.5 and 55.2 ± 3.7 days p...

Elephant movement patterns in relation to surface water demonstrate that they are a water-dependent species. Thus, there has been interest in using surface water management to mitigate problems associated with localized elephant overabundance. However, the physiological mechanisms underlying the elephant's water dependence remain unclear. Although...

Many species respond to increases in environmental noise by increasing the amplitude, duration, and/or repetition rate of their vocalizations. Potential costs of noise-induced vocal modifications include increased energetic costs but no empirical data in marine mammals exist. This study's objective was to compare the metabolic costs of communicativ...

The spatial scale at which organisms respond to human activity can affect both ecological function and conservation planning. Yet little is known regarding the spatial scale at which distinct behaviors related to reproduction and survival are impacted by human interference. Here we provide a novel approach to estimating the spatial scale at which a...