Things that go bump in the night: evolutionary interactions between cephalopods and cetaceans in the tertiary
Abstract
Echolocation has evolved independently in several vertebrate groups, and hypotheses about the origin of echolocation in these groups often invoke abiotic mechanisms driving morphological evolution. In bats, for example, the ecological setting associated with the origin of echolocation has been linked to global warming during the Palaeocene–Eocene; similarly, the origin of toothed whales (odontocetes) has been broadly correlated with the establishment of the circum‐Antarctic current. These scenarios, and the adaptational hypotheses for the evolution of echolocation with which they are associated, neglect a consideration of possible biotic mechanisms. Here we propose that the origin of echolocation in odontocetes was initially an adaptation for nocturnal epipelagic feeding – primarily on diel migrating cephalopods. We test this hypothesis using data on the temporal, geographical, and water column distributions of odontocetes and cephalopods, and other global events from their respective tertiary histories. From this analysis, we suggest that echolocation in early odontocetes aided nocturnal feeding on cephalopods and other prey items, and that this early system was exapted for deep diving and hunting at depths below the photic zone where abundant cephalopod resources were available 24 h a day. This scenario extends to the evolution of other cephalopod feeding (teuthophagous) marine vertebrates such as pinnipeds and Mesozoic marine reptiles.
Keywords
Echolocation has evolved independently in several vertebrate groups, including tenrecs, bats, shrews, toothed whales, and birds (Speakman 2001; Thomas & Jalili 2004). The best known exemplars are microchiropteran bats and odontocete cetaceans, although evolutionary investigations typically highlight different aspects of the origin of echolocation in these two groups. In bats, morphological changes associated with the evolution of the biosonar apparatus are seldom preserved and the fossil record provides few clues towards understanding how echolocation evolved in this group. Phylogenetic analyses using both molecular and morphological data have been compared with the known stratigraphic occurrences of the available fossils, and the resulting concordance broadly suggests a linkage between the Palaeocene–Eocene Thermal Maximum (Gingerich 2006) and the evolution of echolocation in chiropterans (Springer et al. 2001). In comparison to the sparse chiropteran fossil record, the cetacean fossil record is fairly good (Uhen & Pyenson 2002). For odontocetes, the sequence of cranial modifications associated with the evolution of echolocation (and attendant sensory systems) is well preserved in the cetacean fossil record and these transformations have been the focus of detailed evolutionary study (Cranford et al. 1996; Nummela et al. 2004; Marino et al. 2004; Uhen 2004; Pyenson & McKenna 2006). Nonetheless, the ecological context of the evolution of echolocation and specific drivers that influenced the innovation of this complex sensory system has not been addressed.
The Eocene origin of bats has been linked to global warming and the concordant diversification of flowering plants and flying insects bringing ancestral bats into contact with a rich and an unexploited nocturnal food resource (Teeling et al. 2005). The evolution of echolocating odontocetes has been similarly connected to global climate change at the Eocene–Oligocene boundary, namely the establishment of the circum‐Antarctic current and the emergence of the Southern Ocean (Fordyce 1980, 1992, 2003). However, a selective regime associated with this event has only been generally identified, including selection for locating and capturing prey in turbid river waters or as a key attribute that allowed odontocetes to invade and feed at depths below the photic zone (Norris 1968; Norris & Møhl 1983; Pilleri 1990; Fordyce 2003; Thomas & Jalili 2004).
The first scenario is falsified by the ancestral habitat of the earliest odontocetes which, like their ancestors (derived basilosaurids), was probably pelagic, not estuarine. Therefore, an intermediate freshwater stage is not a prerequisite for the evolution of echolocation and it appears to have occurred in a strictly pelagic stem lineage. As currently framed, the second scenario outlines an obvious opportunity for pelagic cetaceans, but it neglects to provide a chronology of putative ecological interactions between odontocetes and their prey resources through time.
We begin by observing that mesopelagic feeding provides access to a diverse array of cephalopods prey resources that, as measured by biomass, surpasses nearly all other prey items in abundance (Boyle & von Boletzky 1996). Today, cephalopods constitute a food source for 90% of all odontocete species (Clarke 1996). Additionally, oceanic odontocetes include taxa (e.g. Physeter, Ziphiidae) that feed almost exclusively on cephalopods (Clarke 1996) and that are also the deepest divers (Schreer & Kovacs 1997) (Fig. 1). But how did early odontocetes gain access to the abundant cephalopod resources found deep in the darkened water column? Did deep‐diving drive the evolution of echolocation or vice versa?
We then examine the palaeoecological setting in which odontocetes evolved echolocation using data from fossil and living odontocete and cephalopod species. Our analysis suggests that the dispersal of Palaeogene cetaceans from marine coastal areas into pelagic waters brought odontocete ancestors into contact with diel migrating cephalopods – abundant prey at or close to the surface, albeit only at night. Thus, the origin of echolocation was not associated with blindly diving into the lightless depths or foraging in dark, turbid waters. Rather, echolocation‐assisted nocturnal hunting conferred a selective advantage over locating epipelagic prey (albeit bioluminescent) with only the aid of moon or star light.
Methods
To establish parameters of the ecological setting in which echolocation evolved in odontocete whales we examined: (1) the chronology and timing of morphological transformations associated with the evolution of echolocation in odontocetes; (2) stratigraphic and palaeogeographical occurrences of the earliest odontocetes; and (3) diving and feeding depths of recent taxa. We compared these data with similar data for cephalopods, including: (1) phylogenetic distribution of diel migration; (2) stratigraphic and palaeogeographical occurrences of tertiary cephalopods, especially members of the Nautiloida; and (3) migration depth ranges of recent taxa. We also compared cetacean, cephalopod and nautiloid generic diversity through the tertiary. These methods follow other palaeobiological investigations that evaluated potential evolutionary interactions that arise out of ecological interactions (e.g. Gould & Calloway 1980, Krause 1986).
Cetaceans
Cetacean genera were compiled from McKenna & Bell's (1997) compendium of mammalian genera. Although the taxonomic completeness of the compendium has been questioned (see Fordyce & Muizon 2001), we use it here because no other generic tabulation was available to us at this time. We added a stratigraphic revision for Odobenocetops (Muizon & Domning 2001), but otherwise left the stratigraphic ranges of the taxa unchanged. We did not tabulate genera with questionable ranges (e.g. Pontobasileus: ?Eocene, ?Oligocene). Cetacean genera were tallied in 13 time bins (Table 1). In addition, we included mysticetes in some of our analyses because most mysticetes also include cephalopods as part of their diet (Gaskin 1976; Evans 1987).
| Palaeocene | Eocene | Oligocene | Miocene | Pliocene | Pleistocene | |||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Early | Late | Early | Middle | Late | Early | Late | Early | Middle | Late | Early | Late | |||
| Cetacea | n = 255 | 4 | 15 | 6 | 4 | 32 | 32 | 90 | 64 | 29 | 15 | 33 | ||
| % genera | 1.6 | 5.9 | 2.4 | 1.6 | 12.5 | 12.5 | 35.3 | 25.1 | 11.4 | 5.9 | 12.9 | |||
| Cephalopoda | n = 38 | 11 | 13 | 17 | 18 | 13 | 12 | 6 | 6 | 7 | 7 | 4 | 8 | 8 |
| % genera | 28.9 | 34.2 | 44.7 | 47.3 | 34.2 | 31.6 | 15.8 | 15.8 | 18.4 | 18.4 | 10.5 | 21.1 | 21.1 | |
| Nautilida | n = 14 | 10 | 10 | 11 | 10 | 10 | 7 | 5 | 3 | 3 | 3 | 1 | 1 | 1 |
| % genera | 71.4 | 71.4 | 78.6 | 71.4 | 71.4 | 50.0 | 35.7 | 21.4 | 21.4 | 21.4 | 7.1 | 7.1 | 7.1 | |
| Sepiida | n = 18 | 1 | 3 | 6 | 7 | 2 | 3 | 2 | 3 | 3 | 2 | 2 | 2 | |
| % genera | 5.6 | 16.7 | 33.3 | 38.9 | 11.1 | 16.7 | 11.1 | 16.7 | 16.7 | 11.1 | 11.1 | 11.1 | ||
| Teuthida | n = 6 | 1 | 1 | 2 | 1 | 1 | 1 | 1 | 1 | 5 | 5 | |||
| % genera | 16.7 | 16.7 | 33.3 | 16.7 | 16.7 | 16.7 | 16.7 | 16.7 | 83.3 | 83.3 | ||||
The available marine rock record probably biases generic diversity (Raup 1976), but the current cetacean fossil record likely provides a fairly accurate picture of cetacean diversity during the tertiary. Even accounting for collection effort, publication effort, and available rock outcrop area, the Middle Miocene remains the apex of cetacean diversity. The Oligocene, however, remains inadequately sampled, probably because of the paucity of marine rock outcrop from this time (Uhen & Pyenson 2002). Moreover, the abundance of unnamed and undescribed Oligocene taxa that exist in several palaeontological collections further biases Palaeogene cetacean diversity towards an underestimate of actual diversity.
Our cetacean phylogeny is a conservative composite of extant odontocete relationships based on several phylogenetic analyses of nuclear and mitochondrial sequence data (Hamilton et al. 2001; Nikaido et al. 2001; Arnason et al. 2004; and May‐Collado & Arnarsson 2006). We did not include extinct odontocete taxa because the relationships among extinct odontocetes and their place among crown odontocete lineages remain contentious and unclear (contrast Fordyce 2002 with Geisler & Sanders 2003). Furthermore, we did not include any of the ‘river dolphin’ lineages because they do not feed on cephalopods (except for Pontoporia) (Clarke 1996; Evans 1987). Although some results have left the relationships among delphinoids unresolved, a majority has resolved phocoenids and delphinids as sister clades to the exclusion of monodontids, which we follow here.
Cephalopods
Our cephalopod phylogeny is based on the combined morphological and molecular analysis of Lindgren et al. (2004). Within cephalopods we highlighted the nautiloids because they are better represented in the fossil record than soft‐bodied cephalopods and, given their morphology, were likely prey items (see below). Genera were compiled from the electronic version of Sepkoski's (2002) compendium of marine metazoans. We selected all genera with ranges in the tertiary, including those with questionable (e.g. ‘?tertiary’) ranges. ‘Eocene’ and ‘?Eocene’ were both coded as extending for the whole Eocene (Early, Middle and Late). ‘Eo–m–l’ was coded as late Eocene. The geological ranges of these genera were also tallied into 13 time bins. Frequency of cetacean and cephalopod genera in the tertiary was calculated using the number of genera per epoch divided by the total number of known genera (Table 1).
Results
Cetaceans
The evolution of echolocation in odontocetes can be recognized by a number of different lines of morphological evidence. In the transition from terrestrial to obligate existences, the earliest cetaceans evolved underwater hearing. The presence and morphology of acoustically isolated ear bones in basilosaurid archaeocetes indicates that the ancestors of all living cetaceans had directional underwater hearing at low‐ to mid‐frequencies by the late middle Eocene (ca. 40 Ma) (Fleischer 1976; Luo & Gingerich 1999; Uhen 2004). By the early Oligocene (33.9–28.4 Ma), the basic sound‐generating biosonar apparatus was in place (Barnes et al. 2001; Fordyce 2003; Pyenson & McKenna 2006). These changes also coincide with the first major encephalization increase in the cetaceans (Marino et al. 2003; Marino et al. 2004), suggesting that the neurological structure to accommodate a complex echolocation system was also in place by the early Oligocene.
Cetaceans had dispersed well beyond Tethys Sea by the late middle Eocene, and it is likely that pelagic basilosaurid archeocetes also encountered cephalopods. However, these early cetaceans did not have an echolocation system (Uhen 2004; Pyenson & McKenna 2006) and they have none of the osteological characters (see Rommel et al. 2006) that are associated with the capacity to dive below the photic zone.
Palaeogene odontocetes are reported from early Oligocene rocks of the northeastern Pacific, and by the end of the Oligocene, odontocetes are well represented in the southwestern Pacific Ocean, the northwestern Atlantic Ocean and the Paratethys Sea (Fordyce 2003), demonstrating that the dispersal routes of the early odontocetes included transoceanic travel. Thus, early odontocetes were morphologically provisioned for echolocation at the same time that pelagic wanderings placed them in the realm of diel migrating cephalopods.
Cephalopods
Diel migrating behaviour is widely distributed among living cephalopods, and likely pre‐dates the origin of the cetaceans by over 340 Ma (Fig. 2). Based on sister group comparisons, diel migration was present in the common ancestor of nautiloids, ammonoids, and coeleoids (octopods, cuttlefish and squid) (Fig. 2). Migration in the water column is absent in living Octopoda, the bathypelagic Vampyromorphida, and most cuttlefish (Idiosepiida and Sepiidae) (Roper & Young 1975), but it occurs predominately among oceanic Teuthida (Fig. 2). As illustrated in Figure 2, benthic octopus do not display diel migration in the water column, but they often have diel activity patterns, being more active at night then during the day (Boyle & Rodhouse 2005). The predominately coastal cuttlefish (Sepiida and Idiosepiida) bury themselves in the sediment during the day and emerge at night to feed (Roper & Young 1975).
Although epipelagic cephalopod resources greatly vary on a diurnal/nocturnal cycle, mesopelagic cephalopod resources are typically less variable in both abundance and biomass than the surface waters (Roper & Young 1975; Moiseev 1991; Nesis & Nikitina 1995), and, as a result, the mesopelagic realm is an advantageous destination for echolocating odontocetes.
Prior to the appearance of echolocation in the early odontocetes, cephalopod diversity returned to its highest level since the terminal Cretaceous–Tertiary (K–T) extinction of the ammonites and other groups. The appearance of odontocetes coincides with a Palaeogene reduction in cephalopod diversity, including a substantial loss of nautiloid taxa, the only cephalopods with external shells to survive the K–T extinction event. Palaeogene nautiloids were broadly distributed in tropical and temperate seas (Kummel 1956) and they show a stable diversity through the Palaeocene, with a small diversification in the early Eocene (Fig. 3). However, generic diversity dwindled from an Eocene high of nine to three genera by the end of the Oligocene, and today six or fewer species assignable to two genera survive on fore reefs in the tropical Indo‐Pacific.
Discussion
Diel migration enriches species diversity, abundance and biomass of cephalopods near the surface of oceanic waters at night. Thirty seven per cent of 62 diel migrating species are found within 100 m of the surface at night, but during the day a depth of 500 m is required to account for 36.8% of the same species diversity (Fig. 1). Compared to daylight hours, abundance and biomass of cephalopods in the epipelagic zone at night can be as much as 10.6 and 4.7 times greater, respectively (Nesis & Nikitina 1995). The trophic significance of abundant cephalopods at the surface at night can also be observed in the diet of non‐diving, nocturnal feeding seabirds (e.g. albatross (Croxall & Prince 1994) and petrals (Imber 1995)) that include some live taken ‘deep water’ cephalopod species.
We suggest that echolocation in early odontocetes aided nocturnal feeding on cephalopods and other prey items, and that this early system was an exaptation for hunting deeper at light poor depths where abundant cephalopod resources were available 24 h a day. Of course, not all living odontocetes dive deep into the mesopelagic (Fig. 1), but the hypothesized intermediate step of nocturnal feeding remains present in many shallow‐diving odontocete species today (Evans 1987; Schreer & Kovacs 1997).
Monks (2002) suggested that if the hollow, gas‐filled, external nautiloid shells produced stronger echoes than soft‐bodied cephalopods, Palaeogene nautiloids would have been highly ‘visible’ prey for early echolocating odontocetes and that this vulnerability may have been responsible for their near demise (Fig. 3). Acoustical studies of the target strength of various shapes and materials, as well as the presence of gas inclusions, support this hypothesis (Urick 1983). Furthermore, the occurrence of highly reflective nautiloids along with the less reflective soft‐bodied coleoids in surface waters would have reduced the necessary sophistication of the earliest echolocating systems, while still providing a morphological base on which the modern system could evolve.
In the Oligocene, odontocetes also transitioned from heterodont (incisors, canines, premolars and molars) to more homodont (uniform peg‐like teeth) dentition (Fordyce 2003; Uhen 2004; Pyenson 2005). The homodonty of some early odontocetes, like Simocetus (Fordyce 2002), was ill suited for durophagy on nautiloids, but it has been suggested that homodonty, concomitant with the size reduction of individual teeth, may have allowed suction feeding to have been widely employed as a feeding strategy in these early odontocetes. A parsimonious interpretation of the phylogenetic distribution of suction feeding in extant lineages (Werth 2006) suggests that suction feeding evolved once along the stem lineage of odontocetes (if not all crown cetaceans). Because the crown node of Odontoceti is at least 31–33 Ma (Simocetus age data from Prothero et al. 2001, p. 190), the advent of suction feeding in odontocetes is consistent with the decline of shelled prey observed in the late Oligocene.
Although this scenario emphasizes cephalopods as prey, fish also constitute an important component in odontocete diets (Gaskin 1976; Evans 1987), and because some fish also undertake diel migration [e.g. Myctophidae or lantern fishes (Watanabe et al. 1999)], these lineages may have had a possible role in our scenario. Although this important prey taxon is present throughout the tertiary, its major diversification did not take place until the Neogene (Sepkoski 2002). In addition, physiological constraints associated with swim bladders make rapid vertical movement difficult (Alexander 1972). Because of this limitation, cephalopods are thought to be more important in vertic niches in the sea – niches that are maintained through daily vertical migration (Webber et al. 2000). Based on these two observations we therefore considered the vertical contribution of fish as prey in this scenario to be ancillary to the role of the cephalopods.
Mysticetes, the sister taxa to odontocetes, offer a striking contrast in the scenario proposed here. All of the morphological evidence to date suggests that echolocation evolved once along the stem of Odontoceti (Pyenson & McKenna 2006); in contrast, mysticetes never have echolocated (Fitzgerald 2006). Most mysticetes migrate substantial distances to find large abundances of their prey (Gaskin 1976; Evans 1987) and, as divers, appear to be limited to epipelagic depths exclusively (Croll et al. 2001). Odontocetes instead find one of their main prey items by diving down the water column, and the deepest divers are also the largest members of the clade (Fig. 1; Schreer & Kovacs 1997). Over evolutionary time, the interactions between cetaceans and cephalopods may qualify as a form of escalation (sensu Vermeij 1987), with the most spectacular example observed in the adult body sizes of the deepest diving and largest echolocating cetacean (Physeter) and its largest prey item, the giant squid (Architeuthis) (Kubodera & Mori 2005).
Diel migrating cephalopod stocks may have also been important in the evolution of other mesopelagic marine predators that do not echolocate (Whitehead et al. 2003). Like cetaceans, off‐shore foraging pinnipeds such as elephant seals (Mirounga sp.) are descended from terrestrial re‐entrants that moved out into the oceanic realm from nearshore habitats (Berta et al. 2006). Thus, like the odontocetes ~15 Ma earlier, the earliest pinnipeds would have also encountered more abundant cephalopods in nocturnal surface waters. Relative to other phocids and otariids, elephant seals have a visual system adapted for low light levels (Schusterman et al. 2000), and an initial increase in visual acuity in their phocid ancestors to feed on diel migrating cephalopods would have served as an exaptation to hunt cephalopod prey at depth as well. Today, elephant seals are the deepest diving pinnipeds (Schreer & Kovacs 1997), and they feed on cephalopods (Klages 1996). Oceanic, large‐eyed billfishes (Istiophoridae or Xiphiidae) are also deep‐diving cephalopod feeders (Smale 1996) and they may have also followed a similar evolutionary pathway. Lastly, the enlargement of the eye sockets in Mesozoic parvipelvian ichthyosaurs may not have been an adaptation for deep diving (Motani et al. 1999), but rather an adaptation for nocturnal feeding on diel migrating ammonoids and other cephalopods in Mesozoic waters.
This study proposes that biotic interactions between cetaceans and cephalopods have played a role in advent of echolocation in odontocetes, as well as shaping the tertiary histories of both groups. We do not deny the impact of abiotic drivers in (e.g. tectonic or climate change), but we have highlighted the importance of biotic, ecological interactions between clades over geological timescales. The possible convergent evolution of echolocation to locate abundant prey at night in both terrestrial (Speakman 2001) and aquatic habitats (as argued here) emphasizes the power of selection to repeatedly generate complex and integrated morphological sensory systems.
In terrestrial habitats echolocation has also provided some groups (e.g. bats and birds) with access to the lightless depths of predator‐free caves, while in aquatic habitats, early odontocetes followed their prey into formerly predator‐free depths by refining the same echolocation mechanism that initially evolved for nocturnal hunting near the surface. Lastly, while the study of the structures associated with echolocation in odontocetes has provided important insights into the morphological evolution of this group, the context in which the structural alterations have taken place is also important. And just as the intermediate or previous uses are necessary for understanding and testing scenarios for evolving morphology, intermediate or previous contexts must also be viable in the reconstruction of evolutionary history.
Conclusion
We have advanced a scenario for the evolution of echolocation in toothed whales (odontocetes) based on a palaeobiological approach similar to that used to explore the context of the evolution of echolocation in bats. Our analyses suggest that echolocation initially provided a selective advantage to detect pelagic prey items (primarily cephalopods) that were migrating to epipelagic waters at night during the Palaeogene. Subsequent modifications and sophistication of the early biosonar system, as documented in the fossil record, were driven by Oligocene odontocetes hunting deeper in the water column as they followed diel migrating prey into lightless depths. All available palaeontological, phylogenetic, ecological and evolutionary data that we have been able to identify and examine do not refute this hypothesis, and it remains viable for further testing.
Acknowledgements
We thank A. Berta, R. Dudley, J.A. Estes and T.M. Williams for their comments and criticism of earlier drafts of this manuscript. R.L. Caldwell, J. Goldbogen, N. Hallinan, R.B. Irmis, M.F. McKenna, S.N. Patek, E.A. Perotti, W.F. Ponder, L. Pyenson, R. Rohde, Y. Valles and J. Voight provided us with helpful insights and discussions. R.E. Fordyce and an anonymous reviewer provided constructive and thought‐provoking comments that greatly improved the quality of this manuscript. D.L. Ashliman helped us with the etymology of the title. This work was supported, in part, by the R. Kellogg and D. & S.P. Welles funds of the University of California Museum of Paleontology (UCMP) and a NSF Graduate Research Fellowship to NDP. This is UCMP contribution no. 1903.
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