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Feeding in Marine Mammals: an Integration of Evolution and Ecology Through Time

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Feeding in Marine Mammals: an Integration of Evolution and Ecology Through Time Palaeontologia Electronica palaeo-electronica.org Feeding in marine mammals: An integration of evolution and ecology through time Annalisa Berta and Agnese Lanzetti ABSTRACT Marine mammals are key components of aquatic ecosystems. Feeding strategies identified in extant cetaceans, pinnipeds, sirenians, marine otters, and polar bears are associated with anatomical specializations of the head (rostrum, palate, temporoman- dibular joint, teeth/baleen, mandible). Genetic and ontogenetic evidence of skull and tooth morphology provide the mechanisms that underlie patterns of feeding diversity. Based on a comprehensive diversity data set derived from the Paleobiology Database, we considered feeding strategies (suction, biting, filter feeding, grazing), prey type (squid, fish, benthic invertebrates, zooplankton, tetrapods, sea grasses), tooth pattern and cusp shape (homodont, heterodont, pointed, rounded, edentulous), and habitat (marine, riverine, estuarine) in fossil and extant marine mammals. These variables were then tested for correlation and their changes through time examined in relation to productivity and climate variables. We provide an integrated analysis of the evolution of feeding and trophic structure in marine mammals and explore the origin and timing of particular feeding strategies over the last 50 million years. In agreement with earlier reports, updated generic counts reveal that the greatest diversity of pinnipedimorphs and cetaceans occurred during the late Miocene (Tortonian), following the Mid-Miocene Climatic Optimum. These historical data are used as a framework to inform past and present structure and trophic interactions and enable predictions about future marine ecosystems.The driv- ers of diet and feeding patterns are both environmental (sea level fluctuations, climate change) and biotic (anatomical specializations, competition, predator-prey). The influ- ence of these processes on paleodiversity varies depending on taxonomic group, tim- ing, and geographic scale. Annalisa Berta. Department of Biology, San Diego State University, San Diego, California 92182, USA. [email protected] Agnese Lanzetti. Department of Biology, San Diego State University, San Diego, California 92182, USA. [email protected] Keywords: marine mammals; diversity curves; feeding strategies; biotic and environmental drivers Berta, Annalisa and Lanzetti, Agnese. 2020. Feeding in marine mammals: An integration of evolution and ecology through time. Palaeontologia Electronica, 23(2):a40. https://doi.org/10.26879/951 palaeo-electronica.org/content/2020/3136-feeding-in-marine-mammals Copyright: August 2020 Paleontological Society. This is an open access article distributed under the terms of Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0), which permits users to copy and redistribute the material in any medium or format, provided it is not used for commercial purposes and the original author and source are credited, with indications if any changes are made. creativecommons.org/licenses/by-nc-sa/4.0/ BERTA & LANZETTI: FEEDING IN MARINE MAMMALS Submission: 7 December 2020. Acceptance: 11 August 2020. INTRODUCTION ecology of feeding in marine mammals. We begin by examining feeding strategies in extant and Marine mammals comprise a diverse assem- extinct marine mammals by associating these blage of at least seven distinct evolutionary lin- strategies with anatomical specializations of the eages that independently returned to the sea and head. We next consider genetic and ontogenetic spend the majority of their time in water. They evidence of skull and tooth morphology, which occupy aquatic ecosystems ranging from the poles underlies the evolution of feeding types. Finally, to the equator and riverine, estuarine, and a variety using key morphological features, we performed a of marine environments from shallow coastal to comprehensive analysis of the evolution of feeding deep sea. Across this diverse range of habitats diversity and trophic structure in marine mammals. they occupy almost every trophic level from top Also incorporated in this framework is evidence predators to primary consumers. In addition to the from diatoms diversity, stable isotopes (e.g., δ18O, three major extant lineages that include pinnipeds δ13C), and sea level changes which track changes (seals, sea lions, and walruses), cetaceans, odon- in productivity, diet, and the environment over geo- tocetes [toothed whales], mysticetes [baleen logic time. whales] and sirenians (manatees and dugongs), other marine mammals include sea otters and Feeding Strategies and Prey polar bears plus several entirely extinct lineages: Marine mammals have evolved multiple feed- desmostylians, aquatic sloths, and an aquatic bear ing strategies to capture and consume food or prey (Berta, 2017). underwater. We have adopted the three feeding Today marine mammals include 130 living categories of extant aquatic predators identified by species (Committee on Taxonomy, 2017). Marine Kienle et al. (2017): biting, suction, and filter feed- mammals have been on Earth for a little more than ing with the addition of a fourth category, grazing to 50 million years, and their past diversity includes include sirenians (Figure 1). It should be noted more than 450 genera (Paleobiology Database, that, like most animals, marine mammals are see Materials and Methods). All of their ancestors opportunistic feeders and capture prey as effi- had well-developed limbs and feet and lived in ter- ciently as possible, which may require them to restrial environments. The transition from land to switch between prey types depending on their sea involved the acquisition of many diverse adap- availability, and they also employ combinations of tations including the ability to capture and consume these strategies (Hocking et al., 2013, 2017a, b; prey in the marine environment. Environmental Kienle et al., 2017). Furthermore, many species pressures involved in foraging in water, such as show variation in foraging strategy that can be increased pressure, density, and viscosity, have related to age, sex, season, and prey type (Kienle resulted in morphological specializations related to and Berta, 2016). locomotion, prey capture, and food processing. Biting. Biting (raptorial) feeding, a common marine The objective of this study is to provide an mammal feeding strategy, can be divided into three integrative analysis of the anatomy, evolution, and FIGURE 1. Feeding strategies of extant marine mammal predators (from Kienle et al., 2017) with the addition of graz- ing (sirenians, authors’ work). 2 PALAEO-ELECTRONICA.ORG subcategories: crushing, grip-and-tear, and pierce swim slowly through dense patches of prey with feeding (Kienle et al., 2017). Crushing is performed open mouths, and prey passively enter the oral when prey is fragmented by the teeth during inges- cavity (Werth and Potvin, 2016). This strategy is tion and intraoral processing. This strategy is best exemplified by balaenid whales (bowhead and exemplified by sea otters (Enhydra lutris) using the right whales). Intermittent filter feeders actively molars to break down hard shelled prey (e.g., sea engulf a single mouthful of prey and remove water urchins, crustaceans, and molluscs). Grip-and-tear using various filtering structures during a distinct feeding defines animals that hold prey with the water removal stage. Intermittent filter feeding can jaws/forelimbs, shake prey and/or rip off smaller be further subdivided into lunge and suction filter pieces during ingestion. This strategy has also feeding based on the method of ingestion (Hocking been documented in some pinnipeds (e.g., leopard et al., 2017a; Kienle et al., 2017). Lunge filter feed- seals Hydrurga leptonyx), some odontocetes (e.g., ing (also called intermittent ram filter feeding, gulp- killer whales Orcinus orca), polar bears (Ursus ing, and ram gulping) is best exemplified by maritimus), and sea otters (Adam and Berta, 2002; balaenopterid whales (e.g., minke, fin, humpback, Kienle and Berta, 2016). In pierce feeding, animals blue, and sei whales also known as rorquals) that bite prey during ingestion, often swallowing prey swim rapidly at a prey patch while opening their whole with little manipulation or external process- mouths to draw in prey (Goldbogen et al., 2010; ing. Suction can be used in combination with both Werth and Ito, 2017). In suction filter feeding, ani- pierce and grip-and-tear feeding to pull prey inside mals such as some phocid seals (e.g., crabeater the mouth. Pierce and suction feeding are seen in seal Lobodon carcinophaga, and leopard seal most pinnipeds (e.g., Weddell seal Leptonychotes Hydrurga leptonyx) use suction to pull prey from weddellii, Hawaiian monk seal Neomonachus the water (e.g., Adam and Berta, 2002; Hocking et schauinslandi), and delphinid odontocetes al., 2013; Kienle and Berta, 2016; Kienle et al., (Stenella, Delphinus, and Tursiops spp.) (Werth, 2017). Lateral suction filter feeding (also called 2006a; Kienle et al., 2015). benthic suction feeding) is a specialized strategy Suction. Suction feeding is the most common seen in the gray whale (Eschrichtius robustus). It feeding strategy seen in aquatic vertebrates includ- involves gray whales rolling laterally onto their right ing fish, sea birds, turtles, and some marine mam- sides and sucking in prey, primarily amphipods, mals (Werth, 2000; Kienle et al., 2017). Suction expelling water and sediment through the baleen feeders generate negative pressure within the oral (El Adli et al.,
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