Dynamic Species Distribution Models in the Marine Realm: Predicting Year-Round Habitat Suitability of Baleen Whales in the Southern Ocean

Species distribution models (SDMs) relate species information to environmental conditions to predict potential species distributions. The majority of SDMs are static, relating species presence information to long-term average environmental conditions. The resulting temporal mismatch between species information and environmental conditions can increase model inference’s uncertainty. For SDMs to capture the dynamic species-environment relationships and predict near-real-time habitat suitability, species information needs to be spatiotemporally matched with environmental conditions contemporaneous to the species’ presence (dynamic SDMs). Implementing dynamic SDMs in the marine realm is highly challenging, particularly due to species and environmental data paucity and spatiotemporally biases. Here, we implemented presence-only dynamic SDMs for four migratory baleen whale species in the Southern Ocean (SO): Antarctic minke, Antarctic blue, fin, and humpback whales. Sightings were spatiotemporally matched with their respective daily environmental predictors. Background information was sampled daily to describe the dynamic environmental conditions in the highly dynamic SO. We corrected for spatial sampling bias by sampling background information respective to the seasonal research efforts. Independent model evaluation was performed on spatial and temporal cross-validation. We predicted the circumantarctic year-round habitat suitability of each species. Daily predictions were also summarized into bi-weekly and monthly habitat suitability. We identified important predictors and species suitability responses to environmental changes. Our results support the propitious use of dynamic SDMs to fill species information gaps and improve conservation planning strategies. Near-real-time predictions can be used for dynamic ocean management, e.g., to examine the overlap between habitat suitability and human activities. Nevertheless, the inevitable spatiotemporal biases in sighting data from the SO call for the need for improving sampling effort in the SO and using alternative data sources (e.g., passive acoustic monitoring) in future SDMs. We further discuss challenges of calibrating dynamic SDMs on baleen whale species in the SO, with a particular focus on spatiotemporal sampling bias issues and how background information should be sampled in presence-only dynamic SDMs. We also highlight the need to integrate visual and acoustic data in future SDMs on baleen whales for better coverage of environmental conditions suitable for the species and avoid constraints of using either data type alone.

Comparing Uncertainty Associated With 1-, 2-, and 3D Aerial Photogrammetry-Based Body Condition Measurements of Baleen Whales

Body condition is a crucial and indicative measure of an animal’s fitness, reflecting overall foraging success, habitat quality, and balance between energy intake and energetic investment toward growth, maintenance, and reproduction. Recently, drone-based photogrammetry has provided new opportunities to obtain body condition estimates of baleen whales in one, two or three dimensions (1D, 2D, and 3D, respectively) – a single width, a projected dorsal surface area, or a body volume measure, respectively. However, no study to date has yet compared variation among these methods and described how measurement uncertainty scales across these dimensions. This associated uncertainty may affect inference derived from these measurements, which can lead to misinterpretation of data, and lack of comparison across body condition measurements restricts comparison of results between studies. Here we develop a Bayesian statistical model using known-sized calibration objects to predict the length and width measurements of unknown-sized objects (e.g., a whale). We use the fitted model to predict and compare uncertainty associated with 1D, 2D, and 3D photogrammetry-based body condition measurements of blue, humpback, and Antarctic minke whales – three species of baleen whales with a range of body sizes. The model outputs a posterior predictive distribution of body condition measurements and allows for the construction of highest posterior density intervals to define measurement uncertainty. We find that uncertainty does not scale linearly across multi-dimensional measurements, with 2D and 3D uncertainty increasing by a factor of 1.45 and 1.76 compared to 1D, respectively. Each standardized body condition measurement is highly correlated with one another, yet 2D body area index (BAI) accounts for potential variation along the body for each species and was the most precise body condition metric. We hope this study will serve as a guide to help researchers select the most appropriate body condition measurement for their purposes and allow them to incorporate photogrammetric uncertainty associated with these measurements which, in turn, will facilitate comparison of results across studies.

Molecular Evolutionary Analyses of Tooth Genes Support Sequential Loss of Enamel and Teeth in Baleen Whales (Mysticeti)

The loss of teeth and evolution of baleen racks in Mysticeti was a profound transformation that permitted baleen whales to radiate and diversify into a previously underutilized ecological niche of bulk filter-feeding on zooplankton and other small prey. Ancestral state reconstructions suggest that teeth were lost in the common ancestor of crown Mysticeti. Genomic studies provide some support for this hypothesis and suggest that the genetic toolkit for enamel production was inactivated in the common ancestor of living baleen whales. However, molecular studies to date have not provided direct evidence for the complete loss of teeth, including their dentin component, on the stem mysticete branch. Given these results, several questions remain unanswered: (1) Were teeth lost in a single step or did enamel loss precede dentin loss? (2) Was enamel lost early or late on the stem mysticete branch? (3) If enamel and dentin/tooth loss were decoupled in the ancestry of baleen whales, did dentin loss occur on the stem mysticete branch or independently in different crown mysticete lineages? To address these outstanding questions, we compiled and analyzed complete protein-coding sequences for nine tooth-related genes from cetaceans with available genome data. Seven of these genes are associated with enamel formation (ACP4, AMBN, AMELX, AMTN, ENAM, KLK4, MMP20) whereas two other genes are either dentin-specific (DSPP) or tooth-specific (ODAPH) but not enamel-specific. Molecular evolutionary analyses indicate that all seven enamel-specific genes have inactivating mutations that are scattered across branches of the mysticete tree. Three of the enamel genes (ACP4, KLK4, MMP20) have inactivating mutations that are shared by all mysticetes. The two genes that are dentin-specific (DSPP) or tooth-specific (ODAPH) do not have any inactivating mutations that are shared by all mysticetes, but there are shared mutations in Balaenidae as well as in Plicogulae (Neobalaenidae + Balaenopteroidea). These shared mutations suggest that teeth were lost at most two times. Shared inactivating mutations and dN/dS analyses, in combination with cetacean divergence times, were used to estimate inactivation times of genes and by proxy enamel and tooth phenotypes. The results of these analyses are most compatible with a two-step model for the loss of teeth in the ancestry of living baleen whales: enamel was lost very early on the stem Mysticeti branch followed by the independent loss of dentin (and teeth) in the common ancestors of Balaenidae and Plicogulae, respectively. These results imply that some stem mysticetes, and even early crown mysticetes, may have had vestigial teeth comprised of dentin with no enamel. Our results also demonstrate that all odontocete species (in our study) with absent or degenerative enamel have inactivating mutations in one or more of their enamel genes.

High Encephalization in a Fossil Rorqual Illuminates Baleen Whale Brain Evolution

Baleen whales are considered underencephalized mammals due to their reduced brain size with respect to their body size (encephalization quotient [EQ] &#x3c;&#x3c; 1). Despite their low EQ, mysticetes exhibit complex behavioral patterns in terms of motor abilities, vocal repertoire, and cultural learning. Very scarce information is available about the morphological evolution of the brain in this group; this makes it difficult to investigate the historical changes in brain shape and size in order to relate the origin of the complex mysticete behavioral repertoire to the evolution of specific neural substrates. Here, the first description of the virtual endocast of a fossil balaenopterid species, <i>Marzanoptera tersillae</i> from the Italian Pliocene, reveals an EQ of around 3, which is exceptional for baleen whales. The endocast showed a morphologically different organization of the brain in this fossil whale as the cerebral hemispheres are anteroposteriorly shortened, the cerebellum lacks the posteromedial expansion of the cerebellar hemispheres, and the cerebellar vermis is unusually reduced. The comparative reductions of the cerebral and cerebellar hemispheres suggest that the motor behavior of <i>M. tersillae</i> probably was less sophisticated than that exhibited by the extant rorqual and humpback species. The presence of an EQ value in this fossil species that is around 10 times higher than that of extant mysticetes opens new questions about brain evolution and provides new, invaluable information about the evolutionary path of morphological and size change in the brain of baleen whales.

Sounds of Stress: Assessment of Relationships between Ambient Noise, Vessel Traffic, and Gray whale Stress Hormone

Elevated noise from human activities in nature can impact animal behavior and physiology, with subsequent impacts on individual health and population dynamics. Baleen whale communication, navigation, habitat use, and ability to recognize and locate prey and predators may be impaired by anthropogenic activities that increase ocean noise within the whales' hearing frequency range. To understand the physiological impacts of noise disturbance on baleen whales, we investigated the adrenal stress response of gray whales (Eschrichtius robustus) to variable ambient noise levels through an assessment of fecal glucocorticoid metabolite concentrations. This analysis was conducted at the individual level, at multiple temporal scales (1-7 days), and accounted for factors that may confound glucocorticoid hormone concentrations: sex, age, nutritional status, and reproductive state. Data were collected along the Oregon coast, USA, from June to October of 2016-2018. Results indicate a significant positive correlation between underwater noise levels and vessel traffic. Vessel counts from the day prior to fecal sample collection and sex had significant positive relationships with glucocorticoid metabolite concentrations. This study increases knowledge of gray whale physiological response to variable ocean noise and may inform management decisions regarding regulations of anthropogenic noise activities and thresholds near critical whale habitats.

Morphological variation of the relictual alveolar structures in the mandibles of baleen whales

Living baleen whales (mysticetes) are bulk filter feeders that use keratinous baleen plates to filter food from prey laden water. Extant mysticetes are born entirely edentulous, though they possess tooth buds early in ontogeny, a trait inherited from toothed ancestors. The mandibles of extant baleen whales have neither teeth nor baleen; teeth are resorbed in utero and baleen grows only on the palate. The mandibles of extant baleen whales also preserve a series of foramina and associated sulci that collectively form an elongated trough, called the alveolar groove. Despite this name, it remains unclear if the alveolar groove of edentulous mysticetes and the dental structures of toothed mammals are homologous. Here, we describe and quantify the anatomical diversity of these structures across extant mysticetes and compare their variable morphologies across living taxonomic groups (i.e., Balaenidae, Neobalaenidae, Eschrichtiidae, and Balaenopteridae). Although we found broad variability across taxonomic groups for the alveolar groove length, occupying approximately 60–80 percent of the mandible’s total curvilinear length (CLL) across all taxa, the relictual alveolar foramen showed distinct patterns, ranging between 15–25% CLL in balaenids, while ranging between 3–12% CLL in balaenopterids. This variability and the morphological patterning along the body of the mandible is consistent with the hypothesis that the foramina underlying the alveolar groove reflect relictual alveoli. These findings also lay the groundwork for future histological studies to examine the contents of these foramina and clarify their potential role in the feeding process.

Cetaceans Sightings During Research Cruises in Three Remote Atlantic British Overseas Territories

Marine mammal sightings were recorded during research cruises to three remote, mid-ocean British Overseas Territories in the South Atlantic and Southern Ocean. In March to April 2018 and 2019, the Exclusive Economic Zones (EEZs) of tropical St Helena and temperate Tristan da Cunha were surveyed. The sub-polar waters of South Georgia and the South Sandwich Islands (SGSSI) were surveyed in February to March 2019. At St Helena in 2018, five species were recorded during 11 sightings, and in 2019, four species, with one additional unidentified species, during seven sightings. Most of these sightings were of dolphin species, which are known to be resident around the Island and seamounts. In Tristan da Cunha in 2018, a total of five identified and one unidentified species were recorded during six sightings, half of which were associated with the Islands or seamounts. In 2019, due to rough weather, no sightings were recorded in the Tristan da Cunha waters. Around SGSSI, 162 sightings of 236 cetaceans were made in 2019, mostly of baleen whales, with seven species identified with certainty. Sightings around the southern South Sandwich Islands included beaked whales and large dolphins, whereas baleen whales dominated in the northern South Sandwich Islands. These results provide new data for rarely surveyed regions, helping to build a spatial picture of important areas for marine mammals, which will help inform marine spatial protection strategies.