Robin C. Dunkin

Vocal performance affects metabolic rate in dolphins: implications for animals communicating in noisy environments

ABSTRACT 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 increasingly noisy habitats. For this investigation, we tested the hypothesis that an increase in vocal effort would result in an energetic cost to the signaler by experimentally measuring oxygen consumption during rest and a 2 min vocal period in dolphins that were trained to vary vocal loudness across trials. Vocal effort was quantified as the total acoustic energy of sounds produced. Metabolic rates during the vocal period were, on average, 1.2 and 1.5 times resting metabolic rate (RMR) in dolphin A and B, respectively. As vocal effort increased, we found that there was a significant increase in metabolic rate over RMR during the 2 min following sound production in both dolphins, and in total oxygen consumption (metabolic cost of sound production plus recovery costs) in the dolphin that showed a wider range of vocal effort across trials. Increases in vocal effort, as a consequence of increases in vocal amplitude, repetition rate and/or duration, are consistent with behavioral responses to noise in free-ranging animals. Here, we empirically demonstrate for the first time in a marine mammal, that these vocal modifications can have an energetic impact at the individual level and, importantly, these data provide a mechanistic foundation for evaluating biological consequences of vocal modification in noise-polluted habitats. Summary: Increased vocal effort by bottlenose dolphins has metabolic costs at the individual level, indicating energetic consequences for wild populations of marine mammals communicating in noise-polluted environments.

The metabolic cost of communicative sound production in bottlenose dolphins (Tursiops truncatus)

SUMMARY Bottlenose dolphins (Tursiops truncatus) produce various communicative sounds that are important for social behavior, maintaining group cohesion and coordinating foraging. For example, whistle production increases during disturbances, such as separations of mother–calf pairs and vessel approaches. It is clear that acoustic communication is important to the survival of these marine mammals, yet the metabolic cost of producing whistles and other socials sounds and the energetic consequences of modifying these sounds in response to both natural and anthropogenic disturbance are unknown. We used flow-through respirometry to determine whether the metabolic cost of sound production could be quantified in two captive dolphins producing social sounds (whistles and squawks). On average, we found that metabolic rates measured during 2 min periods of sound production were 1.2 times resting values. Up to 7 min were required for metabolism to return to resting values following vocal periods. The total metabolic cost (over resting values) of the 2 min vocal period plus the required recovery period (163.3 to 2995.9 ml O2 or 3279.6 to 60,166.7 J) varied by individual as well as by mean duration of sounds produced within the vocal period. Observed variation in received cumulative sound energy levels of vocalizations was not related to total metabolic costs. Furthermore, our empirical findings did not agree with previous theoretical estimates of the metabolic cost of whistles. This study provides the first empirical data on the metabolic cost of sound production in dolphins, which can be used to estimate metabolic costs of vocal responses to environmental perturbations in wild dolphins.

Climate influences thermal balance and water use in African and Asian elephants: physiology can predict drivers of elephant distribution

SUMMARY 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 elephants water dependence remain unclear. Although thermoregulation is likely an important driver, the relationship between thermoregulation, water use and climate has not been quantified. We measured skin surface temperature of and cutaneous water loss from 13 elephants (seven African, 3768±642 kg; six Asian, 3834±498 kg) and determined the contribution of evaporative cooling to their thermal and water budgets across a range of air temperatures (8–33°C). We also measured respiratory evaporative water loss and resting metabolic heat production on a subset of elephants (N=7). The rate of cutaneous evaporative water loss ranged between 0.31 and 8.9 g min−1 m−2 for Asian elephants and 0.26 and 6.5 g min−1 m−2 for African elephants. Simulated thermal and water budgets using climate data from Port Elizabeth, South Africa, and Okaukuejo, Namibia, suggested that the 24-h evaporative cooling water debt incurred in warm climates can be more than 4.5 times that incurred in mesic climates. This study confirms elephants are obligate evaporative coolers but suggests that classification of elephants as water dependent is insufficient given the importance of climate in determining the magnitude of this dependence. These data highlight the potential for a physiological modeling approach to predicting the utility of surface water management for specific populations.

COCCIDIOIDOMYCOSIS AND OTHER SYSTEMIC MYCOSES OF MARINE MAMMALS STRANDING ALONG THE CENTRAL CALIFORNIA, USA COAST: 1998-2012

Abstract A wide range of systemic mycoses have been reported from captive and wild marine mammals from North America. Examples include regionally endemic pathogens such as Coccidioides and Blastomyces spp., and novel pathogens like Cryptococcus gattii, which appear may have been introduced to North America by humans. Stranding and necropsy data were analyzed from three marine mammal stranding and response facilities on the central California coast to assess the prevalence, host demographics, and lesion distribution of systemic mycoses affecting locally endemic marine mammals. Between 1 January 1998 and 30 June 2012, >7,000 stranded marine mammals were necropsied at the three facilities. Necropsy and histopathology records were reviewed to identify cases of locally invasive or systemic mycoses and determine the nature and distribution of fungal lesions. Forty-one animals (0.6%) exhibited cytological, culture- or histologically confirmed locally invasive or systemic mycoses: 36 had coccidioidomycosis, two had zygomycosis, two had cryptococcosis, and one was systemically infected with Scedosporium apiospermum (an Ascomycota). Infected animals included 18 California sea lions (Zalophus californianus), 20 southern sea otters (Enhydra lutris nereis), two Pacific harbor seals (Phoca vitulina richardsi), one Dalls porpoise (Phocoenoides dalli), and one northern elephant seal (Mirounga angustirostris). Coccidioidomycosis was reported from 15 sea lions, 20 sea otters, and one harbor seal, confirming that Coccidioides spp. is the most common pathogen causing systemic mycosis in marine mammals stranding along the central California coast. We also report the first confirmation of C. gattii infection in a wild marine mammal from California and the first report of coccidioidomycosis in a wild harbor seal. Awareness of these pathogenic fungi during clinical care and postmortem examination is an important part of marine mammal population health surveillance and human health protection. Temporal–spatial overlap may be observed for pathogenic mycoses infecting coastal marine mammals and adjacent human populations.

An Unusual Mortality Event of Harbor Porpoises (Phocoena phocoena) Off Central California: Increase in Blunt Trauma Rather Than an Epizootic

In 2007, the apparent increase in the number of harbor porpoises (Phocoena phocoena) stranding along the central California coast compared to the number of strandings the previous year resulted in the declaration of an Unusual Mortality Event by the National Marine Fisheries Service. A statistically significant increase in strandings occurred in 2008 and 2009, with more than twice the mean annual number of strandings documented per year in the previous decade occurring each year, but then strandings decreased in 2010. No single cause of mortality explained all the strandings, and there were no significant changes in age class or sex of strandings in 2008 and 2009. Trauma, including interspecific aggression and fisheries interactions, was the most common cause of death, and blunt force trauma increased significantly in August through October of 2008 and 2009. Domoic acid toxicosis was documented for the first time in this species. Although the cause of death for many strandings was unidentified, the increase in strandings in 2008-2009 reflects an increase in blunt trauma rather than an epizootic of disease.

Energetic Cost of Behaviors Performed in Response to Vessel Disturbance: One Link in the Population Consequences of Acoustic Disturbance Model

Several studies have shown that cetaceans respond to the physical presence and/or acoustic emissions from marine vessels. For example, cetaceans perform surface-active behaviors (SABs) in response to an increase in the number of and/or close approaches by vessels (Lusseau 2006; Noren et al. 2009; Williams et al. 2002, 2009). SABs are often performed in bouts of one or more behaviors performed sequentially, and the majority of SABs provide both visual and acoustic signals that are important to social marine mammals. Indeed, the use of sound is essential to the survival and reproduction of cetaceans (National Research Council 2003), and because of this, anthropogenic sound exposure in marine mammals is a concern. Individuals may compensate for increased vessel noise by changing the amplitude (Holt et al. 2009; Scheifele et al. 2005), duration (Foote et al. 2004), repetition rate, and/or frequency of the sounds they produce.

Comparing the metabolic costs of different sound types in bottlenose dolphins

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 increased as vocal effort increased, illustrating a modest cost of vocal modification. Using these data, metabolic costs can be extrapolated to more typical (higher) values of free-ranging dolphins and compared among sound types. However, cost comparisons are complicated by important differences in methodology and the acoustic energy output between sound type trials. In this investigation, existing data are analyzed specifically to scale and compare costs with these differences taken into account. Total metabolic cost of sound production was calculated above baseline values in ml O2 and related to vocal effort in dB re 1 μPa2s (adjusted to on-axis source levels)...

Comparative and Cumulative Energetic Costs of Odontocete Responses to Anthropogenic Disturbance

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 behavioral responses for several odontocete species (bottlenose dolphin, killer whale, harbor porpoise, and beaked whales). The energetic costs of species-specific responses to anthropogenic disturbance were then estimated. The energetic impact varies across species and scenarios as well as by behavioral responses. Overall, the cumulative energetic cost of ephemeral behavioral responses (e.g., performing surface active behaviors, modifying acoustic signals) and modifying swim speeds and activity budgets likely increases daily energy expenditure by ≤4%. In contrast, the reduction in foraging activity in the presence of vessels and/or exposure to sonar has the potential to significantly reduce individuals’ daily energy acquisition. Indeed, across all odontocete species, decreased energy acquisition as a result of reduced foraging undoubtedly has a larger impact on individuals than the increased energy expenditure associated with behavioral modification. This work provides a powerful tool to investigate the biological significance of multiple behavioral responses that are likely to occur in response to anthropogenic disturbance.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 behavioral responses for several odontocete species (bottlenose dolphin, killer whale, harbor porpoise, and beaked whales). The energetic costs of species-specific responses to anthropogenic disturbance were then estimated. The energetic impact varies across species and scenarios as well as by behavioral responses. Overall, the cumulative energetic cost of ephemeral behavioral responses (e.g., performing surface active behaviors, modifying acoustic signals) and modifying swim speeds and activity budgets likely increases daily energy expenditure by ≤4%. In contrast, the reduction in foraging activity in the presence of vessels and/or exposure to sonar has the potential ...

The metabolic costs of producing clicks and social sounds differ in bottlenose dolphins (Tursiops truncatus)

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 but this prediction is complicated by the fact that clicks are generated at much higher signal intensities. We used flow-through respirometry methods to measure metabolic costs of social sound and click production in two bottlenose dolphins. For all signal types, metabolic rates were related to the energy content of the signals produced. When metabolic costs were compared for equal energy sound generation, clicks were produced at negligible costs relative to resting and at a fraction of the cost of social sound production. However, while the performed repetition rates during click production were similar to field measurements, those of social sounds were much h...

Are there metabolic costs of vocal responses to noise in marine mammals

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 communicative sounds produced by captive bottlenose dolphins (N = 2) under two conditions (low- and high-amplitude vocalization trials) to assess energetic costs of vocal responses to noise. An experimental trial consisted of a 10-min rest period to determine resting metabolic rate, followed by a two-minute vocalization period, and concluded with another 10-min rest period to measure recovery. Open-flow respiratory was used to measure oxygen consumption during each trial component. Vocalizations were recorded using a calibrated hydrophone for analysis. Both dolphins tended to produce longer vocalizations during high-amplitude trials. Thus, metabolic rates were related to to...