Whales and cephalopods in a deep-sea arms race

IF 5.1 2区 地球科学 Q1 LIMNOLOGY Limnology and Oceanography Letters Pub Date : 2024-04-24 DOI:10.1002/lol2.10391
Henk-Jan Hoving, Fleur Visser
{"title":"Whales and cephalopods in a deep-sea arms race","authors":"Henk-Jan Hoving,&nbsp;Fleur Visser","doi":"10.1002/lol2.10391","DOIUrl":null,"url":null,"abstract":"<p>The pelagic deep sea is an enormous three-dimensional space that poses unique selective pressures. In absence of sun light, the dominant forms of communication are bioluminescence and sound. Diverse, abundant taxa inhabit the pelagic deep sea (water column &gt;200 m). These taxa range from microplankton to meganekton, which may aggregate and migrate, resulting in a dynamic system with patches of high biomass—and rich hunting grounds for oceanic predators.</p><p>Toothed whales are mammalian top predators that occur in all oceans. Many of these, including beaked and sperm whales, hunt for deep-sea cephalopods, in particular squids (Clarke <span>2006</span>) (Fig. 1). They have evolved a range of morphological, physiological, and behavioral traits enabling prolonged breath-hold dives to 100 or 1000s of meters (Kooyman <span>2009</span>). Deep-diving toothed whales (i.e., odontocetes routinely foraging deeper than 200 m) are efficient, often generalist predators, daily capturing hundreds of prey (Visser et al. <span>2021</span>). Most cephalopods are fast-growing, relatively short-lived predators with a single reproductive cycle followed by death (semelparity), a life history adaptation that is possibly driven by a massive increase in predation pressure subsequent to the evolutionary loss of the external shell (Amodio et al. <span>2019</span>). Their size and high gonadal investment makes them nutritious prey (Boyle and Rodhouse <span>2005</span>).</p><p>The evolution of cephalopod avoidance strategies is strongly rooted in their response to predominantly visual predators. Cephalopods have co-existed with their main predators, fishes, for 530 million years (Jaitly et al. <span>2022</span>). The much more recent entry of mammals into the marine realm and ensuing evolution of predatory toothed whale echolocation (34 million years ago), created strongly different selective pressures on cephalopod adaptive strategies to avoid predation—this time by acoustic predators. The resulting evolutionary arms race in predator–prey adaptations has shaped the cephalopods and toothed whales into the organisms roaming our modern oceans. Their interactions, however, remain unobserved, and unknown. Have pelagic cephalopods succeeded in eluding large, warm-blooded predators geared for long-range detection of prey? Which traits drive the deep-sea arms race between toothed whales and cephalopods?</p><p>Here, we combine the current knowledge on deep-diving toothed whale predators and their cephalopod prey (focused on oegopsid squids) to reconstruct their sequence of predatory interactions, from search to selection and capture. In the light of current ecological concepts, we form four testable hypotheses supported by research approaches, advancing to a scientific framework that will help understand the selective pressures shaping deep-sea predator–prey systems.</p><p>Cephalopods can sense vibrations using a system analogous to the lateral line system of fishes, and rely on advanced visual capabilities to detect their predators (Jaitly et al. <span>2022</span>). The unusually large eyes of giant squid allow detection of the bioluminescent trail stimulated by approaching whales (Nilsson et al. <span>2012</span>). Histioteuthids, a dominant prey for many toothed whales, have dimorphic eyes. Oriented obliquely in the water column, the large upward-looking eye is likely used to detect prey, and predator silhouettes. The smaller downward-oriented eye visualizes bioluminescent point sources (Thomas et al. <span>2017</span>).</p><p>Marine species avoid predators via various strategies, including gigantism, speed, external defensive structures, crypsis, and schooling. Cephalopod gigantism, as found in giant squid <i>Architeuthis</i> sp. and colossal squid <i>Mesonychoteuthis hamiltoni</i>, is exceptional. Most oceanic squids have mantle lengths &lt;500 mm (Jereb and Roper <span>2010</span>). Although many squids are agile and powerful swimmers (e.g., Gonatidae, Ommastrephidae, Octopoteuthidae), certain taxa have limited escape responses (e.g., Histioteuthidae, Chiroteuthidae). Cephalopod oxygen-binding protein (hemocyanin) is less efficient than the myoglobin of their mammalian predators, leaving them at physiological disadvantage (Seibel <span>2016</span>). The absence of an external shell limits the capacity for physical confrontation. Instead, cephalopod primary defense is to avoid detection, through physical and behavioral crypsis (Jaitly et al. <span>2022</span>).</p><p>To hide in a featureless epipelagic and mesopelagic environment where some light still penetrates, some cephalopods use their mantle for cryptic cover (e.g., <i>Japetella heathi</i> and <i>Onychoteuthis banksi</i>) (Zylinski and Johnsen <span>2011</span>). They can effectively switch between varying degrees of mantle pigmentation, counterillumination, shape and sometimes transparency, to optimize their camouflage to fluctuating light conditions (reviewed in Jaitly et al. <span>2022</span>) and hide from visually attuned predators.</p><p>To avoid predation in the only, and critical reproductive phase, many deep-sea squids (e.g., Cranchiidae, Gonatidae, Histioteuthidae) perform ontogenetic migration (Boyle and Rodhouse <span>2005</span>), resulting in larger individuals occurring deeper, or close to the seafloor. This ontogenetic migration poses a constraint for the mammalian predators, as per their need for oxygen. Once detected, cephalopods may startle or confuse predators, through inking, bioluminescent flashes, retaliation with beaks and armature, or even autotomy (Jaitly et al. <span>2022</span>).</p><p>In the absence of light, toothed whales detect prey using echolocation (e.g., Jensen et al. <span>2018</span>). Irrespective of body size, species have converged on a relatively narrow acoustic beam (the sensory field of view) and hyperallometric investment into sound production structures. Combined, this suggests a strong selective pressure for a sensory system optimized for long-range (i.e., high power), high-resolution detection of individual or patchily distributed prey (Jensen et al. <span>2018</span>). It creates an especially powerful long-range sense, with an estimated detection distance of 100 s of meters for the larger toothed whales (Fais et al. <span>2015</span>; Jensen et al. <span>2018</span>) (Fig. 2). Hunting whales thereby, have a rapid, detailed, and unobstructed overview over large water volumes. In comparison, elephant seals (<i>Mirounga</i> sp.), large nonecholocating marine mammals targeting the deep scattering layer, have a prey detection range of 7–17 m and require foraging trips of more than 100 km to detect sufficient prey (Chevallay et al. <span>2023</span>). Teuthophagous toothed whales use sonar frequencies that have strong energy in the 10–40 kHz band, which is also where some cephalopod species reflect sound most strongly (Benoit-Bird and Lawson <span>2016</span>; Jensen et al. <span>2018</span>). Conversely, provided they share the same general auditory anatomy as their shallow-water relatives, deep-sea cephalopod prey are likely “deaf” toward the echolocation frequencies and remain unaware of remote, approaching whale predators (Wilson et al. <span>2007</span>). The cephalopod will only sense its predator at close range (tens of meters; Fig. 2), visually, or due to particle displacement.</p><p>Deep-diving toothed whales are fast, agile swimmers, sized ~3–18 m, and therefore are larger than terrestrial top predators. A larger body volume enables higher relative oxygen stores and resilience to temperature gradients—larger animals can dive deeper, for longer (Kooyman <span>2009</span>). In the cold deep sea, the homeothermic predators can maintain endurance and fast swimming, providing significant advantage over their poikilothermic prey. These physical and physiological advantages do come at high metabolic costs, demanding many, or large prey (Kooyman <span>2009</span>). Most deep-diving toothed whale species lack functional teeth for feeding and likely ingest complete prey through suction. This puts an upper limit on prey size, exemplified by individuals dying following ingestion of large cephalopods (MacLeod et al. <span>2006</span>; Fernández et al. <span>2017</span>). With some exceptions, toothed whales feed on small prey, 1–5% of their own length, thus depending on the presence of numerous prey (MacLeod et al. <span>2006</span>).</p><p>When a toothed whale searches for and approaches a squid, the interaction between predator and prey takes different shape as a function of distance and mutual capability of detection (Fig. 2). The primary anti-predatory behaviors evolved in cephalopods against visually hunting fish (Jaitly et al. <span>2022</span>) do not suffice for pelagic deep-sea squids eluding echolocating toothed whales. The main sensory systems employed by toothed whales and squids for remote detection, respectively, biosonar and vision, provide a strong advantage for the predatory toothed whale. Their long-range acoustic detection of squids is up to an order of magnitude higher than the presumed maximum visual detection range (e.g., disturbances in the bioluminescent field) of giant squid, which have the largest eyes of all cephalopods (Nilsson et al. <span>2012</span>). Hence, cephalopods are likely under strong selective pressure to avoid remote acoustic detection.\n </p><p>Cephalopods may be able to reduce the possibility of remote detection by minimizing their acoustic cross-section (reflective surface). Similar to fish, many deep-sea squids, have elongated body shapes (Boyle and Rodhouse <span>2005</span>; Jereb and Roper <span>2010</span>) (Fig. 1). While this shape reduces drag, it also results in a small visual silhouette when animals position themselves vertically in the water column, a cryptic position for visual predators that come from above or below (e.g., Miller et al. <span>2014</span>). At the same time, it may be a yet unrecognized defense mechanism in cephalopods against the probability for remote detection by a foraging whale descending from the surface. A vertical position also reduces the acoustic cross-section (detectability), and possibly leads predators to underestimate detected prey size.</p><p>The role of deep-sea squid body posture in reducing remote acoustic detection during the search phase could be tested using an acoustic model estimating squid detectability (i.e., reflecting signal strength) by whale echolocation under varying squid acoustic cross sections and geometry of predator or prey. Given the typically steep dive descents of the acoustic predators, we predict detectability to be significantly reduced in oblique vs. horizontally-oriented squids, when ensonified remotely from above.\n </p><p>While some cephalopods occur in aggregations (e.g., ommastrephids, some species in the deep scattering layer; Benoit-Bird et al. <span>2017</span>), or as mating pairs (Hoving and Vecchione <span>2012</span>), surprisingly, the vast majority of deep-sea cephalopods are observed as single individuals (Hoving et al. <span>2012</span>; Vecchione <span>2019</span>). Biologging records of toothed whale hunting behavior also support non schooling prey. Prey is typically captured during a transitory movement, with capture attempts spaced apart in time and space while the predator moves through its prospect foraging zone. With few exceptions, there is no indication of circling or other movements indicative of backtracking the same area, to target a school (e.g., Fais et al. <span>2015</span>; Aguilar de Soto et al. <span>2020</span>).</p><p>Limited food availability may be an explanation for low prey densities in the deep sea. Single, non schooling individuals, however, are unexpected in a featureless environment, given the apparent evolutionary advantage of group-formation across terrestrial and marine prey taxa, in predator defense (e.g., flocks, schools and herds) (Krause and Ruxton <span>2002</span>). However, schooling may only be an effective strategy against visual, but not acoustic marine predators. Toothed whale foraging decisions are likely strongly driven by prey density, and particularly so as the predators rely on numerous, relatively small prey (MacLeod et al. <span>2006</span>). Schooling will result in enhanced local density and likely enhanced long-range detectability. The high plasticity of the echolocation system allows for high-resolution tracking of single targets (Jensen et al. <span>2018</span>). Hence, schooling could prove detrimental for the pelagic cephalopods. Instead, dispersed individuals may remain below the density threshold and escape pursuit. In this light, it becomes apparent that mating in deep-sea cephalopods might be dangerous, possibly explaining brief, nonselective mating behavior in some (Hoving et al. <span>2012</span>) and sperm storage in most deep-sea squids (Hoving et al. <span>2012</span>; Hoving and Vecchione <span>2012</span>; Vecchione <span>2019</span>). Increased acoustic backscatter from the benthos, limiting the detection by acoustic predators, may have selected for close occurrence and mating near the seafloor (e.g., <i>Pholidoteuthis adami</i>) (Hoving and Vecchione <span>2012</span>). A disadvantage of occurring closer to the seafloor is that escape directions are reduced. We propose that the evolution of long-range acoustic predators shifted predator–prey trade-offs in the deep sea. Schooling posed increased risk to squids, resulting in common occurrence of single individuals.</p><p>Whether dispersal vs. schooling reduces acoustic detection can be assessed through modeling the acoustic detectability of remote dispersed vs. schooling individuals. Cephalopod schooling strategies, that is, whether schooling is modulated as a function of acoustic predator presence, can be tested in field experiments and observations that consider squid schooling behavior preceding known toothed whale predatory interactions. Echo sounders placed close to the prey field, can simultaneously record squids and their cetacean predators, and identify predatory interactions (e.g., Urmy and Benoit-Bird <span>2021</span>). Combining echo sounders with hydrophones will allow the analysis of schooling behavior during predator presence and absence and also during predator search phases with and without ensuing approach and pursuit. Finally, this approach allows analysis of schooling behavior under high vs. low predation pressure. We predict that, if squid dispersal is driven by predation (opposed to environmental drivers), prior to being located, most deep-sea squids will be dispersed (non schooling), and respond to a first cue of an approaching predator presence by further dispersion. We also expect a positive relation between the local level of acoustic predation pressure and the degree of cephalopod dispersion.\n </p><p>If deep-sea cephalopods do not school, how do their mammalian predators maintain efficient foraging on small, remote, and dispersed prey? Deep-diving toothed whales are typically social (24 out of ~26 species), living in cohesive groups. Near-surface spatial proximity is broken, however, during foraging (e.g., Visser et al. <span>2014</span> for pilot whales, <i>Globicephala macrorhynchus</i>)—contrasting the adaptive coordinated hunting of social shallow-diving toothed whales (e.g., Pitman and Durban <span>2012</span> for killer whales, <i>Orcinus orca</i>). For the nine species of deep-diving toothed whales for which foraging strategy has been described, tightly spaced social groups at the surface will spread out over hundreds of meters and hunt synchronously, but individually, at depth. This becomes apparent from (1) the significant increase in inter-individual distance either at surface, or during the dive descent (e.g., Whitehead <span>1989</span>; Aguilar de Soto et al. <span>2020</span>) and (2) from the echolocation signals and movement patterns during foraging dives. These show individual searching and hunting patterns (while other foraging group members can be heard), and no evidence of, for example, joint corralling of prey (e.g., Fais et al. <span>2015</span> for sperm whale <i>Physeter macrocephalus</i>; Aguilar de Soto et al. <span>2020</span> for beaked whales). Synchronization of the foraging effort between group members, recorded across the different deep-diving toothed whale genera, suggests that this is an adaptive strategy that may facilitate detection of prey. This may be achieved through information sharing (reviewed by Hansen et al. <span>2023</span>), and possibly by cover reduction of disturbed cephalopods through behavioral response to another detected predator. Particulate feeding on small prey is a rare foraging strategy in vertebrate social foragers, which typically hunt on individual large, or small schooling prey (Hansen et al. <span>2023</span>). The ratio of predator : prey size predicts the strategy of herding or condensing of prey for deep-diving toothed whales, as observed for, for example, herring-feeding killer whales (Hansen et al. <span>2023</span>). Instead, we propose that a non schooling predator response in cephalopods leads social toothed whales to adopt synchronized, yet individual hunting.</p><p>We predict that coordinated searching and social information transfer between individual predators will increase the energetic efficiency of hunting non schooling deep-sea prey. This can be tested using high-resolution, multisensor tags, or moorings equipped with echo sounders and multihydrophone arrays, which track the positions, acoustic behavior, number of nearby conspecifics and foraging performance of multiple foraging group members (Aguilar de Soto et al. <span>2020</span>; Jang et al. <span>2023</span>), in relation to the prey field (Chevallay et al. <span>2023</span>). We predict that foraging return is higher in individuals that forage in spatiotemporal synchrony than in individuals foraging alone. If foraging-decisions are not socially enhanced, but driven primarily by environmental factors, foraging return will be independent of group size, or reduced, due to competition.\n </p><p>If the predators coordinate their search efforts to overcome cephalopod crypsis, how do cephalopods avoid predation? Given their investment in large, complex eyes, at moderate range (tens of meters) perhaps there is still an option for eluding detection or pursuit, for example, by sensing disturbed conspecifics, adapting orientation, or by exiting the acoustic beam (Fig. 2). However, this may render the individual cephalopod vulnerable for detection by other, nearby-hunting whales. In final pursuit, whales strongly accelerate their biosonar repetition rate and widen their echolocation beam, enabling tracking of rapidly moving nearby targets (Jensen et al. <span>2018</span>). Overall high apparent capture rates (~90%), short sprints and onsets of final approach at only 1–2 predator body lengths (Fais et al. <span>2015</span>; Tønnesen et al. <span>2020</span>; Visser et al. <span>2022</span>), suggest that, once pursued, prey has little chance of escape. Testing this hypothesis requires the documentation of the exact interaction between cephalopod and toothed whale just before capture. To date, these interactions remain unobserved. Escape responses can be studied using whale-mimicking robotics programmed to identify, approach, and follow mesopelagic squids, as has been done for hydromedusae (Yoerger et al. <span>2018</span>). The predatory interaction and potential for escape (or predator success rate), can be studied using high-resolution, multisensor tags which record predator foraging behavior and success, together with the prey field (Chevallay et al. <span>2023</span>) and squid behavior while under attack (Aoki et al. <span>2015</span>). We expect that escape responses include dynamic swimming, inking and bioluminescent displays and that these responses are generally not successful to avoid the acoustic predator.</p><p>The whale-cephalopod system involves interaction between two cognitively advanced animal groups, characterized by apparently strong sensory and physiological advantages for the mammalian predator. Under the unique conditions of the deep ocean environment, the selective pressures that have shaped their adaptive traits differentiate from those in other, well-studied habitats. Specifically, deep-sea cephalopods hunted by whales cannot rely on physical protection or agility and may not find safety in numbers, by schooling. Cephalopod principal “dis-armament” in the foraging interaction with acoustic predators can explain their “live fast die young” strategy (semelparity), highly abundant populations (r-selection), sometimes rapid, nonselective mating behavior, and propensity to seek refuge at large depths (ontogenetic migration). These traits may now allow cephalopods to become increasingly successful in changing oceans with overexploited finfish stocks and rapid warming (Doubleday et al. <span>2016</span>). Whether in response to, or driving whale exceptional sensory capacity and uncommon social foraging strategies, it exemplifies that deep-sea predatory interactions differ from those in better known systems, such as shallow-water and terrestrial systems, and require direct observation to understand their dynamics. We take a critical step in our understanding of deep-sea ecosystem dynamics through identification of predation by whales as a key driver of the life history patterns and density distribution of the abundant and diverse deep-sea cephalopods and advocate a research strategy that considers the selective pressures of the habitat and the well-developed senses of the species.</p><p>None declared.</p>","PeriodicalId":18128,"journal":{"name":"Limnology and Oceanography Letters","volume":null,"pages":null},"PeriodicalIF":5.1000,"publicationDate":"2024-04-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/lol2.10391","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Limnology and Oceanography Letters","FirstCategoryId":"93","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1002/lol2.10391","RegionNum":2,"RegionCategory":"地球科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"LIMNOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

The pelagic deep sea is an enormous three-dimensional space that poses unique selective pressures. In absence of sun light, the dominant forms of communication are bioluminescence and sound. Diverse, abundant taxa inhabit the pelagic deep sea (water column >200 m). These taxa range from microplankton to meganekton, which may aggregate and migrate, resulting in a dynamic system with patches of high biomass—and rich hunting grounds for oceanic predators.

Toothed whales are mammalian top predators that occur in all oceans. Many of these, including beaked and sperm whales, hunt for deep-sea cephalopods, in particular squids (Clarke 2006) (Fig. 1). They have evolved a range of morphological, physiological, and behavioral traits enabling prolonged breath-hold dives to 100 or 1000s of meters (Kooyman 2009). Deep-diving toothed whales (i.e., odontocetes routinely foraging deeper than 200 m) are efficient, often generalist predators, daily capturing hundreds of prey (Visser et al. 2021). Most cephalopods are fast-growing, relatively short-lived predators with a single reproductive cycle followed by death (semelparity), a life history adaptation that is possibly driven by a massive increase in predation pressure subsequent to the evolutionary loss of the external shell (Amodio et al. 2019). Their size and high gonadal investment makes them nutritious prey (Boyle and Rodhouse 2005).

The evolution of cephalopod avoidance strategies is strongly rooted in their response to predominantly visual predators. Cephalopods have co-existed with their main predators, fishes, for 530 million years (Jaitly et al. 2022). The much more recent entry of mammals into the marine realm and ensuing evolution of predatory toothed whale echolocation (34 million years ago), created strongly different selective pressures on cephalopod adaptive strategies to avoid predation—this time by acoustic predators. The resulting evolutionary arms race in predator–prey adaptations has shaped the cephalopods and toothed whales into the organisms roaming our modern oceans. Their interactions, however, remain unobserved, and unknown. Have pelagic cephalopods succeeded in eluding large, warm-blooded predators geared for long-range detection of prey? Which traits drive the deep-sea arms race between toothed whales and cephalopods?

Here, we combine the current knowledge on deep-diving toothed whale predators and their cephalopod prey (focused on oegopsid squids) to reconstruct their sequence of predatory interactions, from search to selection and capture. In the light of current ecological concepts, we form four testable hypotheses supported by research approaches, advancing to a scientific framework that will help understand the selective pressures shaping deep-sea predator–prey systems.

Cephalopods can sense vibrations using a system analogous to the lateral line system of fishes, and rely on advanced visual capabilities to detect their predators (Jaitly et al. 2022). The unusually large eyes of giant squid allow detection of the bioluminescent trail stimulated by approaching whales (Nilsson et al. 2012). Histioteuthids, a dominant prey for many toothed whales, have dimorphic eyes. Oriented obliquely in the water column, the large upward-looking eye is likely used to detect prey, and predator silhouettes. The smaller downward-oriented eye visualizes bioluminescent point sources (Thomas et al. 2017).

Marine species avoid predators via various strategies, including gigantism, speed, external defensive structures, crypsis, and schooling. Cephalopod gigantism, as found in giant squid Architeuthis sp. and colossal squid Mesonychoteuthis hamiltoni, is exceptional. Most oceanic squids have mantle lengths <500 mm (Jereb and Roper 2010). Although many squids are agile and powerful swimmers (e.g., Gonatidae, Ommastrephidae, Octopoteuthidae), certain taxa have limited escape responses (e.g., Histioteuthidae, Chiroteuthidae). Cephalopod oxygen-binding protein (hemocyanin) is less efficient than the myoglobin of their mammalian predators, leaving them at physiological disadvantage (Seibel 2016). The absence of an external shell limits the capacity for physical confrontation. Instead, cephalopod primary defense is to avoid detection, through physical and behavioral crypsis (Jaitly et al. 2022).

To hide in a featureless epipelagic and mesopelagic environment where some light still penetrates, some cephalopods use their mantle for cryptic cover (e.g., Japetella heathi and Onychoteuthis banksi) (Zylinski and Johnsen 2011). They can effectively switch between varying degrees of mantle pigmentation, counterillumination, shape and sometimes transparency, to optimize their camouflage to fluctuating light conditions (reviewed in Jaitly et al. 2022) and hide from visually attuned predators.

To avoid predation in the only, and critical reproductive phase, many deep-sea squids (e.g., Cranchiidae, Gonatidae, Histioteuthidae) perform ontogenetic migration (Boyle and Rodhouse 2005), resulting in larger individuals occurring deeper, or close to the seafloor. This ontogenetic migration poses a constraint for the mammalian predators, as per their need for oxygen. Once detected, cephalopods may startle or confuse predators, through inking, bioluminescent flashes, retaliation with beaks and armature, or even autotomy (Jaitly et al. 2022).

In the absence of light, toothed whales detect prey using echolocation (e.g., Jensen et al. 2018). Irrespective of body size, species have converged on a relatively narrow acoustic beam (the sensory field of view) and hyperallometric investment into sound production structures. Combined, this suggests a strong selective pressure for a sensory system optimized for long-range (i.e., high power), high-resolution detection of individual or patchily distributed prey (Jensen et al. 2018). It creates an especially powerful long-range sense, with an estimated detection distance of 100 s of meters for the larger toothed whales (Fais et al. 2015; Jensen et al. 2018) (Fig. 2). Hunting whales thereby, have a rapid, detailed, and unobstructed overview over large water volumes. In comparison, elephant seals (Mirounga sp.), large nonecholocating marine mammals targeting the deep scattering layer, have a prey detection range of 7–17 m and require foraging trips of more than 100 km to detect sufficient prey (Chevallay et al. 2023). Teuthophagous toothed whales use sonar frequencies that have strong energy in the 10–40 kHz band, which is also where some cephalopod species reflect sound most strongly (Benoit-Bird and Lawson 2016; Jensen et al. 2018). Conversely, provided they share the same general auditory anatomy as their shallow-water relatives, deep-sea cephalopod prey are likely “deaf” toward the echolocation frequencies and remain unaware of remote, approaching whale predators (Wilson et al. 2007). The cephalopod will only sense its predator at close range (tens of meters; Fig. 2), visually, or due to particle displacement.

Deep-diving toothed whales are fast, agile swimmers, sized ~3–18 m, and therefore are larger than terrestrial top predators. A larger body volume enables higher relative oxygen stores and resilience to temperature gradients—larger animals can dive deeper, for longer (Kooyman 2009). In the cold deep sea, the homeothermic predators can maintain endurance and fast swimming, providing significant advantage over their poikilothermic prey. These physical and physiological advantages do come at high metabolic costs, demanding many, or large prey (Kooyman 2009). Most deep-diving toothed whale species lack functional teeth for feeding and likely ingest complete prey through suction. This puts an upper limit on prey size, exemplified by individuals dying following ingestion of large cephalopods (MacLeod et al. 2006; Fernández et al. 2017). With some exceptions, toothed whales feed on small prey, 1–5% of their own length, thus depending on the presence of numerous prey (MacLeod et al. 2006).

When a toothed whale searches for and approaches a squid, the interaction between predator and prey takes different shape as a function of distance and mutual capability of detection (Fig. 2). The primary anti-predatory behaviors evolved in cephalopods against visually hunting fish (Jaitly et al. 2022) do not suffice for pelagic deep-sea squids eluding echolocating toothed whales. The main sensory systems employed by toothed whales and squids for remote detection, respectively, biosonar and vision, provide a strong advantage for the predatory toothed whale. Their long-range acoustic detection of squids is up to an order of magnitude higher than the presumed maximum visual detection range (e.g., disturbances in the bioluminescent field) of giant squid, which have the largest eyes of all cephalopods (Nilsson et al. 2012). Hence, cephalopods are likely under strong selective pressure to avoid remote acoustic detection.

Cephalopods may be able to reduce the possibility of remote detection by minimizing their acoustic cross-section (reflective surface). Similar to fish, many deep-sea squids, have elongated body shapes (Boyle and Rodhouse 2005; Jereb and Roper 2010) (Fig. 1). While this shape reduces drag, it also results in a small visual silhouette when animals position themselves vertically in the water column, a cryptic position for visual predators that come from above or below (e.g., Miller et al. 2014). At the same time, it may be a yet unrecognized defense mechanism in cephalopods against the probability for remote detection by a foraging whale descending from the surface. A vertical position also reduces the acoustic cross-section (detectability), and possibly leads predators to underestimate detected prey size.

The role of deep-sea squid body posture in reducing remote acoustic detection during the search phase could be tested using an acoustic model estimating squid detectability (i.e., reflecting signal strength) by whale echolocation under varying squid acoustic cross sections and geometry of predator or prey. Given the typically steep dive descents of the acoustic predators, we predict detectability to be significantly reduced in oblique vs. horizontally-oriented squids, when ensonified remotely from above.

While some cephalopods occur in aggregations (e.g., ommastrephids, some species in the deep scattering layer; Benoit-Bird et al. 2017), or as mating pairs (Hoving and Vecchione 2012), surprisingly, the vast majority of deep-sea cephalopods are observed as single individuals (Hoving et al. 2012; Vecchione 2019). Biologging records of toothed whale hunting behavior also support non schooling prey. Prey is typically captured during a transitory movement, with capture attempts spaced apart in time and space while the predator moves through its prospect foraging zone. With few exceptions, there is no indication of circling or other movements indicative of backtracking the same area, to target a school (e.g., Fais et al. 2015; Aguilar de Soto et al. 2020).

Limited food availability may be an explanation for low prey densities in the deep sea. Single, non schooling individuals, however, are unexpected in a featureless environment, given the apparent evolutionary advantage of group-formation across terrestrial and marine prey taxa, in predator defense (e.g., flocks, schools and herds) (Krause and Ruxton 2002). However, schooling may only be an effective strategy against visual, but not acoustic marine predators. Toothed whale foraging decisions are likely strongly driven by prey density, and particularly so as the predators rely on numerous, relatively small prey (MacLeod et al. 2006). Schooling will result in enhanced local density and likely enhanced long-range detectability. The high plasticity of the echolocation system allows for high-resolution tracking of single targets (Jensen et al. 2018). Hence, schooling could prove detrimental for the pelagic cephalopods. Instead, dispersed individuals may remain below the density threshold and escape pursuit. In this light, it becomes apparent that mating in deep-sea cephalopods might be dangerous, possibly explaining brief, nonselective mating behavior in some (Hoving et al. 2012) and sperm storage in most deep-sea squids (Hoving et al. 2012; Hoving and Vecchione 2012; Vecchione 2019). Increased acoustic backscatter from the benthos, limiting the detection by acoustic predators, may have selected for close occurrence and mating near the seafloor (e.g., Pholidoteuthis adami) (Hoving and Vecchione 2012). A disadvantage of occurring closer to the seafloor is that escape directions are reduced. We propose that the evolution of long-range acoustic predators shifted predator–prey trade-offs in the deep sea. Schooling posed increased risk to squids, resulting in common occurrence of single individuals.

Whether dispersal vs. schooling reduces acoustic detection can be assessed through modeling the acoustic detectability of remote dispersed vs. schooling individuals. Cephalopod schooling strategies, that is, whether schooling is modulated as a function of acoustic predator presence, can be tested in field experiments and observations that consider squid schooling behavior preceding known toothed whale predatory interactions. Echo sounders placed close to the prey field, can simultaneously record squids and their cetacean predators, and identify predatory interactions (e.g., Urmy and Benoit-Bird 2021). Combining echo sounders with hydrophones will allow the analysis of schooling behavior during predator presence and absence and also during predator search phases with and without ensuing approach and pursuit. Finally, this approach allows analysis of schooling behavior under high vs. low predation pressure. We predict that, if squid dispersal is driven by predation (opposed to environmental drivers), prior to being located, most deep-sea squids will be dispersed (non schooling), and respond to a first cue of an approaching predator presence by further dispersion. We also expect a positive relation between the local level of acoustic predation pressure and the degree of cephalopod dispersion.

If deep-sea cephalopods do not school, how do their mammalian predators maintain efficient foraging on small, remote, and dispersed prey? Deep-diving toothed whales are typically social (24 out of ~26 species), living in cohesive groups. Near-surface spatial proximity is broken, however, during foraging (e.g., Visser et al. 2014 for pilot whales, Globicephala macrorhynchus)—contrasting the adaptive coordinated hunting of social shallow-diving toothed whales (e.g., Pitman and Durban 2012 for killer whales, Orcinus orca). For the nine species of deep-diving toothed whales for which foraging strategy has been described, tightly spaced social groups at the surface will spread out over hundreds of meters and hunt synchronously, but individually, at depth. This becomes apparent from (1) the significant increase in inter-individual distance either at surface, or during the dive descent (e.g., Whitehead 1989; Aguilar de Soto et al. 2020) and (2) from the echolocation signals and movement patterns during foraging dives. These show individual searching and hunting patterns (while other foraging group members can be heard), and no evidence of, for example, joint corralling of prey (e.g., Fais et al. 2015 for sperm whale Physeter macrocephalus; Aguilar de Soto et al. 2020 for beaked whales). Synchronization of the foraging effort between group members, recorded across the different deep-diving toothed whale genera, suggests that this is an adaptive strategy that may facilitate detection of prey. This may be achieved through information sharing (reviewed by Hansen et al. 2023), and possibly by cover reduction of disturbed cephalopods through behavioral response to another detected predator. Particulate feeding on small prey is a rare foraging strategy in vertebrate social foragers, which typically hunt on individual large, or small schooling prey (Hansen et al. 2023). The ratio of predator : prey size predicts the strategy of herding or condensing of prey for deep-diving toothed whales, as observed for, for example, herring-feeding killer whales (Hansen et al. 2023). Instead, we propose that a non schooling predator response in cephalopods leads social toothed whales to adopt synchronized, yet individual hunting.

We predict that coordinated searching and social information transfer between individual predators will increase the energetic efficiency of hunting non schooling deep-sea prey. This can be tested using high-resolution, multisensor tags, or moorings equipped with echo sounders and multihydrophone arrays, which track the positions, acoustic behavior, number of nearby conspecifics and foraging performance of multiple foraging group members (Aguilar de Soto et al. 2020; Jang et al. 2023), in relation to the prey field (Chevallay et al. 2023). We predict that foraging return is higher in individuals that forage in spatiotemporal synchrony than in individuals foraging alone. If foraging-decisions are not socially enhanced, but driven primarily by environmental factors, foraging return will be independent of group size, or reduced, due to competition.

If the predators coordinate their search efforts to overcome cephalopod crypsis, how do cephalopods avoid predation? Given their investment in large, complex eyes, at moderate range (tens of meters) perhaps there is still an option for eluding detection or pursuit, for example, by sensing disturbed conspecifics, adapting orientation, or by exiting the acoustic beam (Fig. 2). However, this may render the individual cephalopod vulnerable for detection by other, nearby-hunting whales. In final pursuit, whales strongly accelerate their biosonar repetition rate and widen their echolocation beam, enabling tracking of rapidly moving nearby targets (Jensen et al. 2018). Overall high apparent capture rates (~90%), short sprints and onsets of final approach at only 1–2 predator body lengths (Fais et al. 2015; Tønnesen et al. 2020; Visser et al. 2022), suggest that, once pursued, prey has little chance of escape. Testing this hypothesis requires the documentation of the exact interaction between cephalopod and toothed whale just before capture. To date, these interactions remain unobserved. Escape responses can be studied using whale-mimicking robotics programmed to identify, approach, and follow mesopelagic squids, as has been done for hydromedusae (Yoerger et al. 2018). The predatory interaction and potential for escape (or predator success rate), can be studied using high-resolution, multisensor tags which record predator foraging behavior and success, together with the prey field (Chevallay et al. 2023) and squid behavior while under attack (Aoki et al. 2015). We expect that escape responses include dynamic swimming, inking and bioluminescent displays and that these responses are generally not successful to avoid the acoustic predator.

The whale-cephalopod system involves interaction between two cognitively advanced animal groups, characterized by apparently strong sensory and physiological advantages for the mammalian predator. Under the unique conditions of the deep ocean environment, the selective pressures that have shaped their adaptive traits differentiate from those in other, well-studied habitats. Specifically, deep-sea cephalopods hunted by whales cannot rely on physical protection or agility and may not find safety in numbers, by schooling. Cephalopod principal “dis-armament” in the foraging interaction with acoustic predators can explain their “live fast die young” strategy (semelparity), highly abundant populations (r-selection), sometimes rapid, nonselective mating behavior, and propensity to seek refuge at large depths (ontogenetic migration). These traits may now allow cephalopods to become increasingly successful in changing oceans with overexploited finfish stocks and rapid warming (Doubleday et al. 2016). Whether in response to, or driving whale exceptional sensory capacity and uncommon social foraging strategies, it exemplifies that deep-sea predatory interactions differ from those in better known systems, such as shallow-water and terrestrial systems, and require direct observation to understand their dynamics. We take a critical step in our understanding of deep-sea ecosystem dynamics through identification of predation by whales as a key driver of the life history patterns and density distribution of the abundant and diverse deep-sea cephalopods and advocate a research strategy that considers the selective pressures of the habitat and the well-developed senses of the species.

None declared.

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鲸鱼和头足类的深海军备竞赛
深海水层是一个巨大的三维空间,具有独特的选择压力。在没有太阳光的情况下,主要的交流方式是生物发光和声音。中上层深海(水柱 200 米)中栖息着种类繁多、数量巨大的类群。这些类群的范围从微小浮游生物到巨型浮游生物,它们可能聚集在一起并进行迁移,从而形成了一个具有高生物量区块的动态系统,也是海洋掠食者的丰富狩猎场。包括喙鲸和抹香鲸在内的许多齿鲸都捕食深海头足类动物,尤其是鱿鱼(Clarke,2006 年)(图 1)。它们已经进化出一系列形态、生理和行为特征,能够长时间憋气潜入 100 或 1000 米深的海底(Kooyman,2009 年)。深潜齿鲸(即日常觅食深度超过 200 米的齿鲸)是高效率的泛食性捕食者,每天捕获数以百计的猎物(Visser 等,2021 年)。大多数头足类都是生长迅速、寿命相对较短的捕食者,只有一个繁殖周期,随后死亡(semelparity),这种生活史适应可能是由于外壳在进化过程中消失后捕食压力大幅增加所导致的(Amodio 等,2019 年)。头足类的体型和高性腺投资使它们成为营养丰富的猎物(Boyle 和 Rodhouse,2005 年)。头足类回避策略的进化主要源于它们对主要是视觉捕食者的反应。头足类与它们的主要捕食者鱼类共存了 5.3 亿年(Jaitly 等,2022 年)。哺乳动物进入海洋领域的时间要晚得多,随之而来的是捕食性齿鲸回声定位的进化(3400 万年前),这对头足类避免捕食的适应性策略造成了强烈不同的选择性压力--这一次是声学捕食者的捕食。由此产生的捕食者-猎物适应性进化军备竞赛将头足类和齿鲸塑造成了漫游于我们现代海洋的生物。然而,它们之间的相互作用仍未被观察到,也不为人知。浮游头足类是否成功地躲避了大型热血掠食者的远距离捕食?哪些特征驱动着齿鲸和头足类之间的深海军备竞赛?在这里,我们结合目前对深潜齿鲸捕食者和它们的头足类猎物(主要是头足类鱿鱼)的了解,重建了它们从搜索到选择和捕获的捕食互动序列。根据当前的生态学概念,我们形成了四个有研究方法支持的可检验假设,并推进到一个科学框架,这将有助于理解塑造深海捕食者-猎物系统的选择性压力。头足类动物可以使用类似于鱼类侧线系统的系统来感知振动,并依靠先进的视觉能力来探测它们的捕食者(Jaitly 等,2022 年)。巨乌贼的眼睛非常大,可以探测到鲸鱼靠近时激发的生物发光痕迹(Nilsson 等,2012 年)。许多齿鲸的主要猎物--Histioteuthids 的眼睛是二形的。大眼睛斜视水体,向上看的眼睛可能用于探测猎物和捕食者的轮廓。海洋物种通过各种策略来躲避捕食者,包括巨型化、速度、外部防御结构、隐身和游弋。头足类的巨型化,如巨型鱿鱼 Architeuthis sp.和巨型鱿鱼 Mesonychoteuthis hamiltoni,是一种特殊的现象。大多数大洋鱿鱼的套管长度为 500 毫米(Jereb 和 Roper,2010 年)。尽管许多鱿鱼都是敏捷而有力的游泳者(例如,鱿科(Gonatidae)、鱿鲂科(Ommastrephidae)、鱿蛸科(Octopoteuthidae)),但某些类群的逃生反应有限(例如,鱿科(Histioteuthidae)、鱿蛸科(Chiroteuthidae))。头足类的氧结合蛋白(血蓝蛋白)不如哺乳动物天敌的肌红蛋白有效,使其处于生理劣势(Seibel,2016 年)。没有外部外壳限制了头足类的身体对抗能力。相反,头足类的主要防御手段是通过物理和行为隐蔽来避免被发现(Jaitly 等,2022 年)。为了躲藏在无特征的上深海和中深海环境中,一些光线仍能穿透,一些头足类利用它们的外壳进行隐蔽(如 Japetella heathi 和 Onychoteuthis banksi)(Zylinski 和 Johnsen,2011 年)。它们可以有效地在不同程度的鳞幔色素、反照、形状(有时是透明度)之间切换,以优化其伪装,适应波动的光照条件(Jaitly 等人 2022 年的综述),躲避视觉敏锐的捕食者。 (Boyle和Rodhouse,2005年),导致较大的个体出现在较深的海底或靠近海底的地方。由于哺乳动物的捕食者需要氧气,这种本体洄游对它们构成了限制。一旦被发现,头足类可能会通过着墨、生物发光闪光、用喙和衔铁报复,甚至自切等方式来惊吓或迷惑捕食者(Jaitly 等,2022 年)。在没有光的情况下,齿鲸利用回声定位来探测猎物(例如,Jensen 等,2018 年)。无论体型大小如何,物种都趋同于相对较窄的声束(感官视野)和对发声结构的超计量投资。这些因素结合在一起,表明感官系统具有强大的选择压力,可优化对单个或零散分布猎物的远距离(即高功率)、高分辨率探测(Jensen 等,2018 年)。它创造了一种特别强大的远距离感官,据估计,大型齿鲸的探测距离可达 100 秒米(Fais 等,2015 年;Jensen 等,2018 年)(图 2)。因此,狩猎鲸可以快速、详细、无障碍地观察到大片水域。相比之下,象海豹(Mirounga sp.)这种以深层散射层为目标的大型非胆囊定位海洋哺乳动物的猎物探测范围为 7-17 米,需要觅食 100 多公里才能探测到足够的猎物(Chevallay 等,2023 年)。嗜喙齿鲸使用的声纳频率在 10-40 kHz 波段具有很强的能量,这也是一些头足类物种对声音反射最强烈的地方(Benoit-Bird 和 Lawson,2016 年;Jensen 等,2018 年)。相反,如果深海头足类猎物的听觉解剖结构与其浅水亲属相同,它们很可能对回声定位频率 "失聪",对远处靠近的鲸鱼捕食者毫无察觉(Wilson 等,2007 年)。头足类只有在近距离(数十米;图 2)、视觉上或由于颗粒位移才会感觉到捕食者。深潜齿鲸是快速、敏捷的游泳者,体型约 3-18 米,因此比陆地顶级捕食者更大。较大的体型可以储存较多的相对氧气,并能适应温度梯度--体型较大的动物可以潜得更深,潜得更久(Kooyman,2009 年)。在寒冷的深海中,恒温掠食者可以保持耐力和快速游动,这为它们战胜恒温猎物提供了显著优势。这些身体和生理优势确实需要付出高昂的新陈代谢代价,需要捕食许多或大型猎物(Kooyman,2009 年)。大多数深潜齿鲸缺乏进食用的功能性牙齿,可能通过吸力摄取完整的猎物。这就对猎物的大小设定了上限,摄入大型头足类后死亡的个体就是例证(MacLeod 等,2006 年;Fernández 等,2017 年)。除个别情况外,齿鲸以自身长度 1-5% 的小型猎物为食,因此取决于是否存在大量猎物(MacLeod 等人,2006 年)。当齿鲸搜寻并接近乌贼时,捕食者与猎物之间的互动会因距离和相互探测能力的不同而呈现出不同的形态(图 2)。头足类进化出的主要反捕食行为是针对目视捕食的鱼类(Jaitly 等,2022 年),但对于躲避回声定位的齿鲸的浮游深海鱿鱼来说,这些行为并不足够。齿鲸和鱿鱼用于远程探测的主要感官系统(分别是生物声纳和视觉)为掠食性齿鲸提供了强大的优势。它们对鱿鱼的远距离声学探测比巨型鱿鱼的假定最大视觉探测范围(如生物发光场中的干扰)高出一个数量级,而巨型鱿鱼的眼睛是所有头足类动物中最大的(Nilsson 等,2012 年)。因此,头足类很可能受到强大的选择压力,以避免远程声学探测。 头足类可能会通过最小化其声学截面(反射面)来降低远程探测的可能性。与鱼类类似,许多深海鱿鱼的体形也是拉长的(Boyle 和 Rodhouse,2005 年;Jereb 和 Roper,2010 年)(图 1)。这种体形在减少阻力的同时,也会导致动物在水体中垂直定位时产生较小的视觉轮廓,这对于来自上方或下方的视觉捕食者来说是一个隐蔽的位置(例如,米勒等人,2014 年)。同时,这也可能是头足类一种尚未被认识到的防御机制,以防止从海面下降的觅食鲸远程探测。垂直位置也会减少声学截面(可探测性),并可能导致捕食者低估探测到的猎物大小。 深海鱿鱼的身体姿态在搜索阶段会降低远程声学探测的作用,可以通过声学模型来测试,该模型可以估计在不同的鱿鱼声学截面和捕食者或猎物的几何形状下,鲸回声定位对鱿鱼的可探测性(即反映信号强度)。考虑到声学捕食者通常会陡峭地下潜,我们预测,当从上方远程发出声音时,斜向鱿鱼与水平向鱿鱼的可探测性会显著降低。 虽然有些头足类动物是聚集在一起的(例如omastrephids,深散射层中的一些物种;Benoit-Bird 等人,2017 年),或者是成对交配的(Hoving 和 Vecchione,2012 年),但令人惊讶的是,绝大多数深海头足类动物都是作为单个个体被观察到的(Hoving 等人,2012 年;Vecchione,2019 年)。齿鲸狩猎行为的生物记录也支持非校食性猎物。猎物通常是在过渡性移动过程中捕获的,捕获尝试在时间和空间上间隔开来,捕食者在其前景觅食区移动。除少数例外情况外,没有迹象表明捕食者会在同一区域盘旋或进行其他运动,以捕捉鱼群(例如,Fais 等,2015 年;Aguilar de Soto 等,2020 年)。然而,考虑到陆地和海洋猎物类群在捕食者防御(如成群、成群和成群)中群体形成的明显进化优势,在无特征环境中单个、不游弋的个体是意料之外的(Krause 和 Ruxton,2002 年)。然而,成群结队可能只是一种有效的策略,用来对付视觉捕食者,而不是声学海洋捕食者。齿鲸的觅食决定很可能受到猎物密度的强烈驱动,尤其是当捕食者依赖大量相对较小的猎物时(MacLeod 等,2006 年)。集群会提高当地密度,并可能提高远距离可探测性。回声定位系统的高度可塑性允许对单一目标进行高分辨率追踪(Jensen 等,2018 年)。因此,缀学可能对浮游头足类不利。相反,分散的个体可能会保持在密度阈值以下,逃避追捕。有鉴于此,深海头足类的交配显然是危险的,这可能解释了某些深海头足类的短暂、非选择性交配行为(Hoving 等,2012 年)和大多数深海鱿鱼的精子储存(Hoving 等,2012 年;Hoving 和 Vecchione,2012 年;Vecchione,2019 年)。来自海底的声学反向散射增加,限制了声学捕食者的探测,这可能选择了在海底附近出现和交配(例如,Pholidoteuthis adami)(Hoving 和 Vecchione,2012 年)。靠近海底出现的一个缺点是逃逸方向减少。我们认为,远距离声学捕食者的进化改变了深海中捕食者与猎物之间的权衡。通过模拟远距离分散与就学个体的声学可探测性,可以评估分散与就学是否会减少声学探测。头足类的求学策略,即求学行为是否会受到声学捕食者存在的影响,可以通过现场实验和观测进行检验,这些实验和观测考虑了已知齿鲸捕食互动之前乌贼的求学行为。将回声测深仪放置在猎物区域附近,可同时记录鱿鱼及其鲸类捕食者,并识别捕食者之间的相互作用(例如,Urmy 和 Benoit-Bird 2021 年)。将回声测深仪与水听器相结合,可以分析捕食者存在和不存在时的游弋行为,以及捕食者搜索阶段的游弋行为,包括随后的接近和追逐。最后,这种方法还可以分析高捕食压力和低捕食压力下的游弋行为。我们预测,如果鱿鱼的散布是由捕食驱动的(而不是环境驱动),那么在被定位之前,大多数深海鱿鱼将是散布的(非学校行为),并通过进一步散布来对捕食者接近的第一个线索做出反应。我们还预计,当地的声学捕食压力水平与头足类的分散程度之间存在正相关关系。 如果深海头足类没有学校,那么它们的哺乳动物捕食者是如何保持对小型、偏远和分散猎物的高效捕食的呢?深潜齿鲸是典型的社会性动物(约 26 种中的 24 种),生活在有凝聚力的群体中。然而,在觅食过程中,近水面的空间接近性会被打破(例如,Visser 等人 2014 年对领航鲸(Globicephala macrorhynchus)的研究)--这与社会性浅潜齿鲸的适应性协调捕食形成鲜明对比(例如,Pitman 和 Durban 2012 年对虎鲸(Orcinus orca)的研究)。 对于已经描述了觅食策略的九种深潜齿鲸来说,在海面上紧密分布的社会群体将分散到数百米的范围内,在深度上同步但单独地觅食。这一点从(1)海面或下潜过程中个体间距离的显著增加(如 Whitehead 1989;Aguilar de Soto 等,2020 年)和(2)下潜觅食过程中的回声定位信号和运动模式中可以明显看出。这些信号显示了个体的搜寻和捕猎模式(同时也能听到其他觅食群体成员的声音),没有证据显示联合围捕猎物等情况(例如,Fais 等人 2015 年对抹香鲸 Physeter macrocephalus 的研究;Aguilar de Soto 等人 2020 年对喙鲸的研究)。在不同的深潜齿鲸属中记录到的群体成员之间的同步觅食努力表明,这是一种适应性策略,可能有助于发现猎物。这可能是通过信息共享实现的(Hansen 等人 2023 年的综述),也可能是通过对另一个被发现的捕食者的行为反应来减少受干扰头足类动物的覆盖。对小型猎物进行微粒捕食是脊椎动物社会性捕食者中一种罕见的捕食策略,它们通常捕食个体较大或小型成群的猎物(Hansen 等,2023 年)。捕食者与猎物大小的比例预示着深潜齿鲸会采取集群或集中捕食猎物的策略,例如在以鲱鱼为食的虎鲸身上观察到的情况(Hansen 等,2023 年)。我们预测,个体捕食者之间的协调搜索和社会信息传递将提高捕食非学校深海猎物的能量效率。可以使用高分辨率、多传感器标签或配备回声探测仪和多水听器阵列的锚系设备来测试这一点,这些设备可以跟踪多个觅食群体成员的位置、声学行为、附近同类的数量和觅食表现(Aguilar de Soto 等,2020 年;Jang 等,2023 年),以及与猎物场的关系(Chevallay 等,2023 年)。我们预测,与单独觅食的个体相比,时空同步觅食的个体的觅食回报率更高。如果觅食决策不是由社会因素增强,而是主要由环境因素驱动,那么觅食回报率将与群体大小无关,或者由于竞争而降低。 如果捕食者协调它们的搜索努力以克服头足类的隐性,头足类如何避免被捕食?考虑到它们在大而复杂的眼睛上的投资,在中等距离(数十米)内,或许仍有躲避探测或追捕的选择,例如,通过感知受干扰的同类、调整方向或退出声波波束(图 2)。然而,这可能会使头足类个体容易被附近的其他捕猎鲸鱼发现。在最后的追逐中,鲸鱼会强烈加快其生物声纳重复率并扩大其回声定位波束,从而能够追踪附近快速移动的目标(詹森等人,2018 年)。总体表观捕获率高(约 90%)、冲刺时间短且最后接近时仅有 1-2 个捕食者体长(Fais 等,2015 年;Tønnesen 等,2020 年;Visser 等,2022 年),这表明猎物一旦被追捕,几乎没有逃脱的机会。要验证这一假设,需要记录头足类与齿鲸在捕获前的确切互动。迄今为止,这些互动仍未被观察到。可以使用模仿鲸的机器人来研究逃逸反应,这种机器人可以识别、接近和跟踪中上层鱿鱼,就像对水蚤所做的那样(Yoerger 等,2018 年)。捕食互动和逃逸潜力(或捕食成功率)可使用高分辨率多传感器标签进行研究,这些标签可记录捕食者的觅食行为和成功率,以及猎物场(Chevallay 等,2023 年)和鱿鱼受攻击时的行为(Aoki 等,2015 年)。我们预计,逃逸反应包括动态游泳、墨迹和生物发光显示,这些反应一般不会成功避开声学捕食者。鲸-头足类系统涉及两个认知先进的动物群体之间的互动,其特点是哺乳动物捕食者明显具有很强的感官和生理优势。在深海环境的独特条件下,形成它们适应性特征的选择性压力不同于其他经过充分研究的栖息地。具体来说,被鲸鱼捕食的深海头足类无法依靠身体保护或敏捷性,也可能无法通过群居找到数量上的安全。
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来源期刊
CiteScore
10.00
自引率
3.80%
发文量
63
审稿时长
25 weeks
期刊介绍: Limnology and Oceanography Letters (LO-Letters) serves as a platform for communicating the latest innovative and trend-setting research in the aquatic sciences. Manuscripts submitted to LO-Letters are expected to present high-impact, cutting-edge results, discoveries, or conceptual developments across all areas of limnology and oceanography, including their integration. Selection criteria for manuscripts include their broad relevance to the field, strong empirical and conceptual foundations, succinct and elegant conclusions, and potential to advance knowledge in aquatic sciences.
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