Marine biology
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Editorial Cite this article: Walther BD, Munguia P, Fuiman LA. 2015 Frontiers in marine movement ecology: mechanisms and consequences of migration and dispersal in marine habitats. Biol. Lett. 11: 20150146. http://dx.doi.org/10.1098/rsbl.2015.0146
Author for correspondence: Benjamin D. Walther e-mail: [email protected]
One contribution to the special feature ‘Frontiers in marine movement ecology’ organized by Lee Fuiman, Benjamin Walther and Pablo Munguia. Invited to commemorate 350 years of scientific publishing at the Royal Society.
Frontiers in marine movement ecology: mechanisms and consequences of migration and dispersal in marine habitats Benjamin D. Walther1, Pablo Munguia2 and Lee A. Fuiman1 1 2
Marine Science Institute, The University of Texas at Austin, Port Aransas, TX 78373, USA School of Biological Sciences, University of Adelaide, Adelaide, South Australia 5005, Australia BW, 0000-0002-2902-4001
Dispersal and migration are important ecological processes that influence rates of propagule exchange, colonization, extinction and speciation for a wide array of taxa in terrestrial and aquatic systems. The role of movement patterns in the marine environment is particularly critical, because a majority of marine species have a mobile phase at some stage of their life history. Indeed, seminal works that lay the foundation of modern ecology as a science recognized the importance of mobility—whether driven by currents or by swimming—to the dynamics of marine communities. The origins of movement ecology can be traced to the HMS Challenger expedition (1872–1876) led by Sir Charles Wyville Thomson, which was the first scientific survey of the world’s oceans. Thomson [1] hypothesized that high dispersal abilities of benthic organisms played a role in homogenizing deep sea communities given that ‘most marine animals pass a longer or shorter period of their lives as minute free-swimming larvae, and while in that condition are borne along and scattered by tides and currents.’ ( p. 39). This perspective persisted, such as in the pioneering 1914 work by Johan Hjort [2] on factors that drive population fluctuations of commercially important fishes. Prior to Hjort’s work, the prevailing theory was that temporal variations in fishery yields were driven primarily by adult migrations, but Hjort’s careful analyses indicated that year-class strengths were, instead, defined by survival through an early life-history ‘critical period’, with survival being dependent in part on larval dispersal [3]. These hypotheses have been altered, expanded, debated, supported and refuted by subsequent generations of marine ecologists. Indeed, regarding larval dispersal, Hjort [2] himself noted, ‘It would be especially desirable to determine the extent of such movement . . . ’ ( p. 206), and this desire has continued throughout the subsequent century. Paradigms about the role of movement and its relative importance at different ontogenetic stages have shifted during recent decades. For example, marine ecology in the 1980s was dominated by ‘supply side’ theory, focusing on the notion that marine populations were limited by recruitment [4], which inspired debates about whether such processes were dependent or independent of population density [5]. The idea that marine populations were well mixed on large spatial scales and therefore fundamentally ‘open’ with respect to dispersal and recruitment began to change at the beginning of the twenty-first century with recognition of potentially significant amounts of self-recruitment and natal homing [6]. This shift to a focus on characterizing degrees of population connectivity among marine metapopulations continues and it underlies many of the papers in this special feature. Despite the long-standing interest in marine dispersal and migration, movement patterns for most species are poorly characterized. The reasons for this lack of knowledge are largely practical. Many species have a dispersive larval
& 2015 The Author(s) Published by the Royal Society. All rights reserved.
Competing interests. The authors have no competing interests.
References 1.
2.
3.
4.
Thomson CW. 1880 Report on the scientific results of the voyage of H.M.S. Challenger during the years 1873 –76. General introduction to the zoological series of reports. London, UK: Longmans & Co. Hjort J. 1914 The fluctuations in the great fisheries of northern Europe viewed in the light of biological research. Rapp. P-v. Reun. Cons. Int. Explor. Mer. 20, 1– 228. Hare JA. 2014 The future of fisheries oceanography lies in the pursuit of multiple hypotheses. ICES J. Mar. Sci. 71, 2343– 2356. (doi:10.1093/icesjms/ fsu018) Gaines S, Roughgarden J. 1985 Larval settlement rate: a leading determinant of structure in an
5.
6.
7.
ecological community of the marine intertidal zone. Proc. Natl Acad. Sci. USA 82, 3707–3711. (doi:10. 1073/pnas.82.11.3707) Hixon MA. 2011 60 Years of coral reef fish ecology: past, present, future. Bull. Mar. Sci. 87, 727–765. (doi:10.5343/bms.2010.1055) Cowen RK, Gawarkiewicz G, Pineda J, Thorrold SR, Werner FE. 2007 Population connectivity in marine systems: an overview. Oceanography 20, 14 –21. (doi:10.5670/oceanog.2007.26) Cagua EF, Cochran JEM, Rohner CA, Prebble CEM, Sinclair-Taylor TH, Pierce SJ, Berumen ML. 2015 Acoustic telemetry reveals cryptic residency of whale sharks. Biol. Lett. 11, 20150092. (doi:10.1098/rsbl. 2015.0092)
8.
Eggleston DB, Millstein E, Plaia G. 2015 Timing and route of migration of mature female blue crabs in a tidal estuary. Biol. Lett. 11, 20140936. (doi:10.1098/ rsbl.2014.0936) 9. Shima JS, Noonburg EG, Swearer SE. 2015 Consequences of variable larval dispersal pathways and resulting phenotypic mixtures to the dynamics of marine metapopulations. Biol. Lett. 11, 20140778. (doi:10.1098/rsbl.2014.0778) 10. Gillanders BM, Izzo C, Doubleday ZA, Ye Q. 2015 Partial migration: growth varies between resident and migratory fish. Biol. Lett. 11, 20140850. (doi:10.1098/rsbl.2014.0850) 11. Shulzitski K, Sponaugle S, Hauff M, Walter K, D’Alessandro EK, Cowen RK. 2015 Close encounters
2
Biol. Lett. 11: 20150146
pathways of highly mobile adult stages. Eggleston et al. [8] identify migratory corridors of adults that link oceanic spawning to estuarine recruitment. Further, White [12] uses a stage-structured model to evaluate the importance of ontogenetic migrations to the design of spatially explicit marine reserves, thereby illustrating the relevance of movement ecology for fishery management and conservation. Coinciding with paradigm shifts from recruitment limitation to connectivity and metapopulation structure, there has been a growing interest in the ecological consequences of individually variable behaviours [16]. Much of this work involves quantifying the degree to which populations are made up of ‘contingents’—groups of individuals that display distinct migratory patterns [17] such as partial migration, whereby populations are composed of migrants and residents. Such migratory diversity can be a critical driver of population resilience to environmental change [18]. Although partial migration has been well recognized in avian and terrestrial insect species, the extension of this conceptual framework to marine organisms has only recently gained traction [19]. In this special feature, Gillanders et al. [10] identify partial migration in estuarine-dependent fishes as a key driver of growth with strong implications for population persistence in dynamic environments. Similarly, Cagua et al. [7] recognize cryptic residency as a crucial but overlooked population component for highly migratory species. These studies emphasize the need for continuing work that evaluates the role of individually variable migratory behaviour in driving population persistence. Efforts to quantify the importance of migratory diversity will benefit from the new electronic technologies and methods of analysing spatial data that are emerging from the field of biologging [20], and the intersection of behavioural diversity and environmental conditions remains a frontier where the mechanisms driving divergent migratory patterns must be explored. Continued work expanding the frontiers of marine movement ecology will be required given that fishery pressure, habitat modification and shifting climatic conditions are altering the structure of marine populations worldwide. Understanding the ecology of migration and dispersal is critical for future efforts to manage spatially structured marine populations in the face of changing environments.
rsbl.royalsocietypublishing.org
stage during which they are small, suffer high mortality rates, and are diluted in large volumes of water, all of which eliminate the possibility of tracking individual larvae in real time from birth to settlement. Species that are highly migratory during juvenile or adult phases can traverse large distances over long time periods, and their oceanic distribution patterns are often unknown. Recent advances in development of a variety of ecological tools, however, have allowed unprecedented insight into movement dynamics, and many of these approaches produced the ecological insights gained by the studies included in this special feature. These include telemetry techniques [7,8] analysis of geochemical signatures in calcified structures [9,10] and targeted sampling using advanced oceanographic technology [11]. Furthermore, models and experiments that explicitly incorporate mobile phases in their design advance our understanding of movement, leading to refinements in theory or improved management of natural systems [12,13]. And finally, new conceptual models about the importance of movement at different life-history stages set the stage for future work [14]. The questions being investigated in marine movement ecology are growing in complexity and sophistication. When characterizing the dispersal dynamics of mobile lifehistory stages, it is no longer sufficient to merely identify dispersal trajectories. Instead, we now ask how environmental conditions intersect with variable dispersal patterns to drive post-settlement recruitment dynamics. This intersection is examined by Shulzitski et al. [15], who link larval growth performance (which is highly correlated with survivorship) with transport in highly productive and prey-replete mesoscale eddies. Similarly, Shima et al. [9] demonstrate that retentive or dispersive pathways have a significant effect on larval growth and energetic condition, with implications for metapopulation persistence. Temporal fluctuations in habitat quality are also critical in spatially structured populations and communities. Using an experimental approach, Munguia [13] shows that, for species with sex-biased dispersal, propagule availability in source populations can have profound effects on demographic characteristics of sink populations. These strong and important short-term dynamics are complemented by research on postlarval movement in soft sediment systems, and Pilditch et al. [14] argue that ‘secondary’ dispersal can be of greater importance to the structure of benthic metacommunities. It is also critical to understand migratory
18. Kerr L, Secor D. 2012 Partial migration across populations of white perch (Morone americana): a flexible life history strategy in a variable estuarine environment. Estuar. Coast 35, 227–236. (doi:10. 1007/s12237-011-9434-2) 19. Chapman BB, Hulthe´n K, Brodersen J, Nilsson PA, Skov C, Hansson LA, Bro¨nmark C. 2012 Partial migration in fishes: causes and consequences. J. Fish. Biol. 81, 456 –478. (doi:10.1111/j.10958649.2012.03342.x) 20. Rutz C, Hays GC. 2009 New frontiers in biologging science. Biol. Lett. 5, 289–292. (doi:10.1098/rsbl. 2009.0089)
3
Biol. Lett. 11: 20150146
Biol. Lett. 11, 20140795. (doi:10.1098/rsbl. 2014.0795) 15. Sponaugle S, Paris C, Walter KD, Kourafalou V, D’Alessandro E. 2012 Observed and modeled larval settlement of a reef fish to the Florida Keys. Mar. Ecol. Prog. Ser. 453, 201–212. (doi:10.3354/Meps09641) 16. Sih A, Cote J, Evans M, Fogarty S, Pruitt J. 2012 Ecological implications of behavioural syndromes. Ecol. Lett. 15, 278–289. (doi:10.1111/j.1461-0248.2011.01731.x) 17. Secor DH. 1999 Specifying divergent migrations in the concept of stock: the contingent hypothesis. Fish. Res. 43, 13 –34. (doi:10.1016/S01657836(99)00064-8)
rsbl.royalsocietypublishing.org
with eddies: oceanographic features increase growth of larval reef fishes during their journey to the reef. Biol. Lett. 11, 20140746. (doi:10.1098/rsbl. 2014.0746) 12. White JW. 2015 Marine reserve design theory for species with ontogenetic migration. Biol. Lett. 11, 20140511. (doi:10.1098/rsbl.2014.0511) 13. Munguia P. 2015 Role of sources and temporal sinks in a marine amphipod. Biol. Lett. 11, 20140864. (doi:10.1098/rsbl.2014.0864) 14. Pilditch CA, Valanko S, Norkko J, Norkko A. 2015 Post-settlement dispersal: the neglected link in maintenance of soft-sediment biodiversity.
rsbl.royalsocietypublishing.org
Editorial Cite this article: Walther BD, Munguia P, Fuiman LA. 2015 Frontiers in marine movement ecology: mechanisms and consequences of migration and dispersal in marine habitats. Biol. Lett. 11: 20150146. http://dx.doi.org/10.1098/rsbl.2015.0146
Author for correspondence: Benjamin D. Walther e-mail: [email protected]
One contribution to the special feature ‘Frontiers in marine movement ecology’ organized by Lee Fuiman, Benjamin Walther and Pablo Munguia. Invited to commemorate 350 years of scientific publishing at the Royal Society.
Frontiers in marine movement ecology: mechanisms and consequences of migration and dispersal in marine habitats Benjamin D. Walther1, Pablo Munguia2 and Lee A. Fuiman1 1 2
Marine Science Institute, The University of Texas at Austin, Port Aransas, TX 78373, USA School of Biological Sciences, University of Adelaide, Adelaide, South Australia 5005, Australia BW, 0000-0002-2902-4001
Dispersal and migration are important ecological processes that influence rates of propagule exchange, colonization, extinction and speciation for a wide array of taxa in terrestrial and aquatic systems. The role of movement patterns in the marine environment is particularly critical, because a majority of marine species have a mobile phase at some stage of their life history. Indeed, seminal works that lay the foundation of modern ecology as a science recognized the importance of mobility—whether driven by currents or by swimming—to the dynamics of marine communities. The origins of movement ecology can be traced to the HMS Challenger expedition (1872–1876) led by Sir Charles Wyville Thomson, which was the first scientific survey of the world’s oceans. Thomson [1] hypothesized that high dispersal abilities of benthic organisms played a role in homogenizing deep sea communities given that ‘most marine animals pass a longer or shorter period of their lives as minute free-swimming larvae, and while in that condition are borne along and scattered by tides and currents.’ ( p. 39). This perspective persisted, such as in the pioneering 1914 work by Johan Hjort [2] on factors that drive population fluctuations of commercially important fishes. Prior to Hjort’s work, the prevailing theory was that temporal variations in fishery yields were driven primarily by adult migrations, but Hjort’s careful analyses indicated that year-class strengths were, instead, defined by survival through an early life-history ‘critical period’, with survival being dependent in part on larval dispersal [3]. These hypotheses have been altered, expanded, debated, supported and refuted by subsequent generations of marine ecologists. Indeed, regarding larval dispersal, Hjort [2] himself noted, ‘It would be especially desirable to determine the extent of such movement . . . ’ ( p. 206), and this desire has continued throughout the subsequent century. Paradigms about the role of movement and its relative importance at different ontogenetic stages have shifted during recent decades. For example, marine ecology in the 1980s was dominated by ‘supply side’ theory, focusing on the notion that marine populations were limited by recruitment [4], which inspired debates about whether such processes were dependent or independent of population density [5]. The idea that marine populations were well mixed on large spatial scales and therefore fundamentally ‘open’ with respect to dispersal and recruitment began to change at the beginning of the twenty-first century with recognition of potentially significant amounts of self-recruitment and natal homing [6]. This shift to a focus on characterizing degrees of population connectivity among marine metapopulations continues and it underlies many of the papers in this special feature. Despite the long-standing interest in marine dispersal and migration, movement patterns for most species are poorly characterized. The reasons for this lack of knowledge are largely practical. Many species have a dispersive larval
& 2015 The Author(s) Published by the Royal Society. All rights reserved.
Competing interests. The authors have no competing interests.
References 1.
2.
3.
4.
Thomson CW. 1880 Report on the scientific results of the voyage of H.M.S. Challenger during the years 1873 –76. General introduction to the zoological series of reports. London, UK: Longmans & Co. Hjort J. 1914 The fluctuations in the great fisheries of northern Europe viewed in the light of biological research. Rapp. P-v. Reun. Cons. Int. Explor. Mer. 20, 1– 228. Hare JA. 2014 The future of fisheries oceanography lies in the pursuit of multiple hypotheses. ICES J. Mar. Sci. 71, 2343– 2356. (doi:10.1093/icesjms/ fsu018) Gaines S, Roughgarden J. 1985 Larval settlement rate: a leading determinant of structure in an
5.
6.
7.
ecological community of the marine intertidal zone. Proc. Natl Acad. Sci. USA 82, 3707–3711. (doi:10. 1073/pnas.82.11.3707) Hixon MA. 2011 60 Years of coral reef fish ecology: past, present, future. Bull. Mar. Sci. 87, 727–765. (doi:10.5343/bms.2010.1055) Cowen RK, Gawarkiewicz G, Pineda J, Thorrold SR, Werner FE. 2007 Population connectivity in marine systems: an overview. Oceanography 20, 14 –21. (doi:10.5670/oceanog.2007.26) Cagua EF, Cochran JEM, Rohner CA, Prebble CEM, Sinclair-Taylor TH, Pierce SJ, Berumen ML. 2015 Acoustic telemetry reveals cryptic residency of whale sharks. Biol. Lett. 11, 20150092. (doi:10.1098/rsbl. 2015.0092)
8.
Eggleston DB, Millstein E, Plaia G. 2015 Timing and route of migration of mature female blue crabs in a tidal estuary. Biol. Lett. 11, 20140936. (doi:10.1098/ rsbl.2014.0936) 9. Shima JS, Noonburg EG, Swearer SE. 2015 Consequences of variable larval dispersal pathways and resulting phenotypic mixtures to the dynamics of marine metapopulations. Biol. Lett. 11, 20140778. (doi:10.1098/rsbl.2014.0778) 10. Gillanders BM, Izzo C, Doubleday ZA, Ye Q. 2015 Partial migration: growth varies between resident and migratory fish. Biol. Lett. 11, 20140850. (doi:10.1098/rsbl.2014.0850) 11. Shulzitski K, Sponaugle S, Hauff M, Walter K, D’Alessandro EK, Cowen RK. 2015 Close encounters
2
Biol. Lett. 11: 20150146
pathways of highly mobile adult stages. Eggleston et al. [8] identify migratory corridors of adults that link oceanic spawning to estuarine recruitment. Further, White [12] uses a stage-structured model to evaluate the importance of ontogenetic migrations to the design of spatially explicit marine reserves, thereby illustrating the relevance of movement ecology for fishery management and conservation. Coinciding with paradigm shifts from recruitment limitation to connectivity and metapopulation structure, there has been a growing interest in the ecological consequences of individually variable behaviours [16]. Much of this work involves quantifying the degree to which populations are made up of ‘contingents’—groups of individuals that display distinct migratory patterns [17] such as partial migration, whereby populations are composed of migrants and residents. Such migratory diversity can be a critical driver of population resilience to environmental change [18]. Although partial migration has been well recognized in avian and terrestrial insect species, the extension of this conceptual framework to marine organisms has only recently gained traction [19]. In this special feature, Gillanders et al. [10] identify partial migration in estuarine-dependent fishes as a key driver of growth with strong implications for population persistence in dynamic environments. Similarly, Cagua et al. [7] recognize cryptic residency as a crucial but overlooked population component for highly migratory species. These studies emphasize the need for continuing work that evaluates the role of individually variable migratory behaviour in driving population persistence. Efforts to quantify the importance of migratory diversity will benefit from the new electronic technologies and methods of analysing spatial data that are emerging from the field of biologging [20], and the intersection of behavioural diversity and environmental conditions remains a frontier where the mechanisms driving divergent migratory patterns must be explored. Continued work expanding the frontiers of marine movement ecology will be required given that fishery pressure, habitat modification and shifting climatic conditions are altering the structure of marine populations worldwide. Understanding the ecology of migration and dispersal is critical for future efforts to manage spatially structured marine populations in the face of changing environments.
rsbl.royalsocietypublishing.org
stage during which they are small, suffer high mortality rates, and are diluted in large volumes of water, all of which eliminate the possibility of tracking individual larvae in real time from birth to settlement. Species that are highly migratory during juvenile or adult phases can traverse large distances over long time periods, and their oceanic distribution patterns are often unknown. Recent advances in development of a variety of ecological tools, however, have allowed unprecedented insight into movement dynamics, and many of these approaches produced the ecological insights gained by the studies included in this special feature. These include telemetry techniques [7,8] analysis of geochemical signatures in calcified structures [9,10] and targeted sampling using advanced oceanographic technology [11]. Furthermore, models and experiments that explicitly incorporate mobile phases in their design advance our understanding of movement, leading to refinements in theory or improved management of natural systems [12,13]. And finally, new conceptual models about the importance of movement at different life-history stages set the stage for future work [14]. The questions being investigated in marine movement ecology are growing in complexity and sophistication. When characterizing the dispersal dynamics of mobile lifehistory stages, it is no longer sufficient to merely identify dispersal trajectories. Instead, we now ask how environmental conditions intersect with variable dispersal patterns to drive post-settlement recruitment dynamics. This intersection is examined by Shulzitski et al. [15], who link larval growth performance (which is highly correlated with survivorship) with transport in highly productive and prey-replete mesoscale eddies. Similarly, Shima et al. [9] demonstrate that retentive or dispersive pathways have a significant effect on larval growth and energetic condition, with implications for metapopulation persistence. Temporal fluctuations in habitat quality are also critical in spatially structured populations and communities. Using an experimental approach, Munguia [13] shows that, for species with sex-biased dispersal, propagule availability in source populations can have profound effects on demographic characteristics of sink populations. These strong and important short-term dynamics are complemented by research on postlarval movement in soft sediment systems, and Pilditch et al. [14] argue that ‘secondary’ dispersal can be of greater importance to the structure of benthic metacommunities. It is also critical to understand migratory
18. Kerr L, Secor D. 2012 Partial migration across populations of white perch (Morone americana): a flexible life history strategy in a variable estuarine environment. Estuar. Coast 35, 227–236. (doi:10. 1007/s12237-011-9434-2) 19. Chapman BB, Hulthe´n K, Brodersen J, Nilsson PA, Skov C, Hansson LA, Bro¨nmark C. 2012 Partial migration in fishes: causes and consequences. J. Fish. Biol. 81, 456 –478. (doi:10.1111/j.10958649.2012.03342.x) 20. Rutz C, Hays GC. 2009 New frontiers in biologging science. Biol. Lett. 5, 289–292. (doi:10.1098/rsbl. 2009.0089)
3
Biol. Lett. 11: 20150146
Biol. Lett. 11, 20140795. (doi:10.1098/rsbl. 2014.0795) 15. Sponaugle S, Paris C, Walter KD, Kourafalou V, D’Alessandro E. 2012 Observed and modeled larval settlement of a reef fish to the Florida Keys. Mar. Ecol. Prog. Ser. 453, 201–212. (doi:10.3354/Meps09641) 16. Sih A, Cote J, Evans M, Fogarty S, Pruitt J. 2012 Ecological implications of behavioural syndromes. Ecol. Lett. 15, 278–289. (doi:10.1111/j.1461-0248.2011.01731.x) 17. Secor DH. 1999 Specifying divergent migrations in the concept of stock: the contingent hypothesis. Fish. Res. 43, 13 –34. (doi:10.1016/S01657836(99)00064-8)
rsbl.royalsocietypublishing.org
with eddies: oceanographic features increase growth of larval reef fishes during their journey to the reef. Biol. Lett. 11, 20140746. (doi:10.1098/rsbl. 2014.0746) 12. White JW. 2015 Marine reserve design theory for species with ontogenetic migration. Biol. Lett. 11, 20140511. (doi:10.1098/rsbl.2014.0511) 13. Munguia P. 2015 Role of sources and temporal sinks in a marine amphipod. Biol. Lett. 11, 20140864. (doi:10.1098/rsbl.2014.0864) 14. Pilditch CA, Valanko S, Norkko J, Norkko A. 2015 Post-settlement dispersal: the neglected link in maintenance of soft-sediment biodiversity.
