skip to main content

Title: Convergence of marine megafauna movement patterns in coastal and open oceans
The extent of increasing anthropogenic impacts on large marine vertebrates partly depends on the animals’ movement patterns. Effective conservation requires identification of the key drivers of movement including intrinsic properties and extrinsic constraints associated with the dynamic nature of the environments the animals inhabit. However, the relative importance of intrinsic versus extrinsic factors remains elusive. We analyze a global dataset of ∼2.8 million locations from >2,600 tracked individuals across 50 marine vertebrates evolutionarily separated by millions of years and using different locomotion modes (fly, swim, walk/paddle). Strikingly, movement patterns show a remarkable convergence, being strongly conserved across species and independent of body length and mass, despite these traits ranging over 10 orders of magnitude among the species studied. This represents a fundamental difference between marine and terrestrial vertebrates not previously identified, likely linked to the reduced costs of locomotion in water. Movement patterns were primarily explained by the interaction between species-specific traits and the habitat(s) they move through, resulting in complex movement patterns when moving close to coasts compared with more predictable patterns when moving in open oceans. This distinct difference may be associated with greater complexity within coastal microhabitats, highlighting a critical role of preferred habitat in shaping marine more » vertebrate global movements. Efforts to develop understanding of the characteristics of vertebrate movement should consider the habitat(s) through which they move to identify how movement patterns will alter with forecasted severe ocean changes, such as reduced Arctic sea ice cover, sea level rise, and declining oxygen content. « less
; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; more » ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; « less
Award ID(s):
Publication Date:
Journal Name:
Proceedings of the National Academy of Sciences
Page Range or eLocation-ID:
3072 to 3077
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    The epaulette shark, Hemiscyllium ocellatum, is a small, reef-dwelling, benthic shark that—using its paired fins—can walk, both in and out of water. Within the reef flats, this species experiences short periods of elevated CO2 and hypoxia as well as fluctuating temperatures as reef flats become isolated with the outgoing tide. Past studies have shown that this species is robust (i.e., respiratory and metabolic performance, behavior) to climate change-relevant elevated CO2 levels as well as hypoxia and anoxia tolerant. However, epaulette shark embryos reared under ocean warming conditions hatch earlier and smaller, with altered patterns and coloration, and with higher metabolic costs than their current-day counterparts. Findings to date suggest that this species has adaptations to tolerate some, but perhaps not all, of the challenging conditions predicted for the 21st century. As such, the epaulette shark is emerging as a model system to understand vertebrate physiology in changing oceans. Yet, few studies have investigated the kinematics of walking and swimming, which may be vital to their biological fitness, considering their habitat and propensity for challenging environmental conditions. Given that neonates retain embryonic nutrition via an internalized yolk sac, resulting in a bulbous abdomen, while juveniles actively forage for worms, crustaceans,more »and small fishes, we hypothesized that difference in body shape over early ontogeny would affect locomotor performance. To test this, we examined neonate and juvenile locomotor kinematics during the three aquatic gaits they utilize—slow-to-medium walking, fast walking, and swimming—using 13 anatomical landmarks along the fins, girdles, and body midline. We found that differences in body shape did not alter kinematics between neonates and juveniles. Overall velocity, fin rotation, axial bending, and tail beat frequency and amplitude were consistent between early life stages. Data suggest that the locomotor kinematics are maintained between neonate and juvenile epaulette sharks, even as their feeding strategy changes. Studying epaulette shark locomotion allows us to understand this—and perhaps related—species’ ability to move within and away from challenging conditions in their habitats. Such locomotor traits may not only be key to survival, in general, as a small, benthic mesopredator (i.e., movements required to maneuver into small reef crevices to avoid aerial and aquatic predators), but also be related to their sustained physiological performance under challenging environmental conditions, including those associated with climate change—a topic worthy of future investigation.

    « less
  2. Synopsis

    Many ecological factors influence animal movement, including properties of the media that they move on or through. Animals moving in terrestrial environments encounter conditions that can be challenging for generating propulsion and maintaining stability, such as inclines and deformable substrates that can cause slipping and sinking. In response, tetrapods tend to adopt a more crouched posture and lower their center of mass on inclines and increase the surface area of contact on deformable substrates, such as sand. Many amphibious fishes encounter the same challenges when moving on land, but how these finned animals modulate their locomotion with respect to different environmental conditions and how these modifications compare with those seen within tetrapods is relatively understudied. Mudskippers (Gobiidae: Oxudercinae) are a particularly noteworthy group of amphibious fishes in this context given that they navigate a wide range of environmental conditions, from flat mud to inclined mangrove trees. They use a unique form of terrestrial locomotion called “crutching,” where their pectoral fins synchronously lift and vault the front half of the body forward before landing on their pelvic fins, while the lower half of the body and tail are kept straight. However, recent work has shown that mudskippers modify some aspectsmore »of their locomotion when crutching on deformable surfaces, particularly those at an incline. For example, on inclined dry sand, mudskippers bent their bodies laterally and curled and extended their tails to potentially act as a secondary propulsor and/or anti-slip device. In order to gain a more comprehensive understanding of the functional diversity and context-dependency of mudskipper crutching, we compared their kinematics on different combinations of substrate types (solid, mud, and dry sand) and inclines (0°, 10°, and 20°). In addition to increasing lateral bending on deformable and inclined substrates, we found that mudskippers increased the relative contact time and contact area of their paired fins, while becoming more crouched, which are responses comparable to those seen in tetrapods and other amphibious fish. Mudskippers on these substrates also exhibited previously undocumented behaviors, such as extending and adpressing the distal portions of their pectoral fins more anteriorly, dorsoventrally bending their trunk, “belly-flopping” on sand, and “gripping” the mud substrate with their pectoral fin rays. Our study highlights potential compensatory mechanisms shared among vertebrates in terrestrial environments while also illustrating that locomotor flexibility and even novelty can emerge when animals are challenged with environmental variation.

    « less
  3. Abstract

    Larger animals studied during ontogeny, across populations, or across species, usually have lower mass-specific metabolic rates than smaller animals (hypometric scaling). This pattern is usually observed regardless of physiological state (e.g., basal, resting, field, and maximally active). The scaling of metabolism is usually highly correlated with the scaling of many life-history traits, behaviors, physiological variables, and cellular/molecular properties, making determination of the causation of this pattern challenging. For across-species comparisons of resting and locomoting animals (but less so for across populations or during ontogeny), the mechanisms at the physiological and cellular level are becoming clear. Lower mass-specific metabolic rates of larger species at rest are due to (a) lower contents of expensive tissues (brains, liver, and kidneys), and (b) slower ion leak across membranes at least partially due to membrane composition, with lower ion pump ATPase activities. Lower mass-specific costs of larger species during locomotion are due to lower costs for lower-frequency muscle activity, with slower myosin and Ca++ ATPase activities, and likely more elastic energy storage. The evolutionary explanation(s) for hypometric scaling remain(s) highly controversial. One subset of evolutionary hypotheses relies on constraints on larger animals due to changes in geometry with size; for example, lower surface-to-volume ratiosmore »of exchange surfaces may constrain nutrient or heat exchange, or lower cross-sectional areas of muscles and tendons relative to body mass ratios would make larger animals more fragile without compensation. Another subset of hypotheses suggests that hypometric scaling arises from biotic interactions and correlated selection, with larger animals experiencing less selection for mass-specific growth or neurolocomotor performance. An additional third type of explanation comes from population genetics. Larger animals with their lower effective population sizes and subsequent less effective selection relative to drift may have more deleterious mutations, reducing maximal performance and metabolic rates. Resolving the evolutionary explanation for the hypometric scaling of metabolism and associated variables is a major challenge for organismal and evolutionary biology. To aid progress, we identify some variation in terminology use that has impeded cross-field conversations on scaling. We also suggest that promising directions for the field to move forward include (1) studies examining the linkages between ontogenetic, population-level, and cross-species allometries; (2) studies linking scaling to ecological or phylogenetic context; (3) studies that consider multiple, possibly interacting hypotheses; and (4) obtaining better field data for metabolic rates and the life history correlates of metabolic rate such as lifespan, growth rate, and reproduction.

    « less
  4. By dispersing seeds long distances, large, fruit-eating animals influence plant population spread and community dynamics. After fruit consumption, animal gut passage time and movement determine seed dispersal patterns and distances. These, in turn, are influenced by extrinsic, environmental variables and intrinsic, individual-level variables. We simulated seed dispersal by forest elephants ( Loxodonta cyclotis ) by integrating gut passage data from wild elephants with movement data from 96 individuals. On average, elephants dispersed seeds 5.3 km, with 89% of seeds dispersed farther than 1 km. The longest simulated seed dispersal distance was 101 km, with an average maximum dispersal distance of 40.1 km. Seed dispersal distances varied among national parks, perhaps due to unmeasured environmental differences such as habitat heterogeneity and configuration, but not with human disturbance or habitat openness. On average, male elephants dispersed seeds farther than females. Elephant behavioral traits strongly influenced dispersal distances, with bold, exploratory elephants dispersing seeds 1.1 km farther than shy, idler elephants. Protection of forest elephants, particularly males and highly mobile, exploratory individuals, is critical to maintaining long distance seed dispersal services that shape plant communities and tropical forest habitat.
  5. Synopsis

    Organisms rely on the integrity of the structural materials they produce to maintain a broad range of processes, such as acquiring food, resisting predators, or withstanding extreme environmental forces. The production and maintenance of these biomaterials, which are often modulated by environmental conditions, can therefore have important consequences for fitness in changing climates. One well-known example of such a biomaterial is mussel byssus, an array of collagen-like fibers (byssal threads) that tethers a bivalve mollusk securely to benthic marine substrates. Byssus strength directly influences mortality from dislodgement, predation, or competition and depends on the quantity and quality of byssal threads produced. We compared the temperature sensitivity of byssal attachment strength of two mussel species common to the west coast of North America, Mytilus trossulus and M. galloprovincialis, when exposed to seawater temperatures ranging from 10 to 24°C in the laboratory. We found that the two species attached equally strong in seawater ≤18°C, but higher temperatures caused byssal thread production rate and quality (break force and extensibility) to be greatly reduced in M. trossulus and increased in M. galloprovincialis, leading to a 2–10-fold difference in overall byssus strength between the two species. Using this threshold value (18°C), we mapped habitat formore »each species along the west coast of North America based on annual patterns in sea surface temperature. Estimated ranges are consistent with the current distribution of the two species and suggest a potential mechanism by which ocean warming could facilitate the northern expansion of M. galloprovincialis and displacement of native M. trossulus populations.

    « less