Drivers of Sex-specific Trade-offs in the Macroalga <i>Ascophyllum nodosum</i>

Martyn Kurr; Andrew John Davies

doi:doi:10.11648/j.plant.20200803.12

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Drivers of Sex-specific Trade-offs in the Macroalga Ascophyllum nodosum

Martyn Kurr, Andrew John Davies

Published in Plant (Volume 8, Issue 3)

Received: 17 July 2020 Accepted: 17 August 2020 Published: 3 September 2020

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Abstract

Little is known about reproductive trade-offs in seaweeds, but sex-specific differences in mortality, production of metabolites, threshold size for reproduction, and susceptibility to herbivory have been reported. The macroalga Ascophyllum nodosum exhibits sex-specific trade-offs at sites where wave-action and herbivory are stronger, because females increase their investment into reproduction at the expense of chemical defences. Females may do this at stressed sites because of high germling and juvenile mortality, or to compensate for lower fecundity due smaller adult sizes at these sites. This study aimed to determine which is the case by comparing A. nodosum in an area where stressors (wave-action and herbivory) impacted upon both adult performance and juvenile mortality, to one where only adult performance was impacted (by ice-damage). Seven populations of the algae were compared at both the regional (> 1000 km) and local scales (< 50 km), to assess the presence of sex-specific differences in algal size, sex-ratio, and the chemical defences and tissue condition of both vegetative and reproductive structures. Taking a multi-scale approach is a useful way to determine which abiotic variables are driving biological patterns, because variability in the latter mirrors variability in the former. Sex-specific trade-offs were more common at both the regional and local scale when herbivory and wave-exposure were high. Other factors caused differences in physiology at both scales, but did not drive sex-specific differences. Furthermore, sex-specific differences were consistent in the defence of reproductive tissues at all sites, suggesting that this was not driven by stress at all. Therefore, sex-specific differences in A. nodosum are caused by some stressors, not caused by others, and are present in some fashion regardless of stress. This is the first study to directly quantify sex-specific trade-offs at different spatial scales in populations of either plants or algae, and as such it reveals novel insights into the driving forces behind them.

Published in	Plant (Volume 8, Issue 3)
DOI	10.11648/j.plant.20200803.12
Page(s)	54-63
Creative Commons	This is an Open Access article, distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution and reproduction in any medium or format, provided the original work is properly cited.
Copyright	Copyright © The Author(s), 2020. Published by Science Publishing Group

Keywords

Chemical Ecology, Dioecy, Intertidal Ecology, Herbivory, Resource Allocation, Stress Responses

References

[1]	Engel, C., Åberg, P., Gaggiotti, O. E., Destombe, C., & Valero, M. (2001). Population dynamics and stage structure in a haploid-diploid red seaweed, Gracilaria gracilis. Journal of Ecology, 89, 436-450.
[2]	Payo, D. A., Colo, J., Calumpong, H., & Clerck, O. D. (2011). Variability of non-polar secondary metabolites in the red alga Portieria. Marine drugs, 9, 2438-2468.
[3]	Viejo, R. M., Martínez, B., Arrontes, J., Astudillo, C., & Hernández, L. (2011). Reproductive patterns in central and marginal populations of a large brown seaweed: drastic changes at the southern range limit. Ecography, 34, 75-84.
[4]	Vergés, A., Paul, N. A. & Steinberg, P. D. (2008). Sex And Life -History Stage Alter 706 Herbivore Responses To A Chemically Defended Red Alga. Ecology, 89, 1334-1343.
[5]	Kurr, M., & Davies, A. J. (2018). Sex-specific reproductive trade-offs in the gregarious fucoid macroalga Ascophyllum nodosum. European Journal of Phycology, 53, 1-13.
[6]	Vernet, P., & Harper, J. L. (1980). The costs of sex in seaweeds. Biological Journal of the Linnean Society, 13, 129-138.
[7]	Delph, L. F., & Herlihy, C. R. (2012). Sexual, fecundity, and viability selection on flower size and number in a sexually dimorphic plant. Evolution, 66, 1154-1166.
[8]	Barrett, S. C., & Hough, J. (2012). Sexual dimorphism in flowering plants. Journal of Experimental Botany, ers308.
[9]	Lazo, L., Markham, J. H., & Chapman, A. R. O. (1994). Herbivory and harvesting: effects on sexual recruitment and vegetative modules of Ascophyllum nodosum. Ophelia, 40, 95-113.
[10]	Dudgeon, S., Kübler, J. E., Wright, W. A., Vadas Sr, R. L., & Petraitis, P. S. (2001). Natural variability in zygote dispersal of Ascophyllum nodosum at small spatial scales. Functional Ecology, 15, 595-604.
[11]	Åberg, P. & Pavia H. (1997). Temporal and multiple scale spatial variation in juvenile and adult abundance of the brown alga Ascophyllum nodosum. Marine Ecology Progress Series, 158, 111-119.
[12]	Vadas, R., Wright, W. A., & Miller, S. L. (1990). Recruitment of Ascophyllum nodosum: wave action as a source of mortality. Marine Ecology-Progress Series, 61, 263-272.
[13]	Cousens, R. (1985). Frond size distributions and the effects of the algal canopy on the behaviour of Ascophyllum nodosum (L.) Le Jolis. Journal of experimental marine biology and ecology, 92, 231-249.
[14]	Toth, G. B., Karlsson, M., & Pavia, H. (2007). Mesoherbivores reduce net growth and induce chemical resistance in natural seaweed populations. Oecologia, 152, 245-255.
[15]	Åberg, P. (1996). Patterns of reproductive effort in the brown alga Ascophyllum nodosum. Marine ecology progress series. Oldendorf, 138, 199-207.
[16]	Pavia, H., Toth, G. B., & Åberg, P. (2002). Optimal defense theory: elasticity analysis as a tool to predict intraplant variation in defenses. Ecology, 83, 891-897.
[17]	Moore, J. C., & Pannell, J. R. (2011). Sexual selection in plants. Current biology, 21, R176-R182.
[18]	Levin, S. A. (1992). The problem of pattern and scale in ecology: the Robert H. MacArthur award lecture. Ecology, 73, 1943-1967.
[19]	Ugarte, R. A. (2011). An evaluation of the mortality of the brown seaweed Ascophyllum nodosum (L.) Le Jol. produced by cutter rake harvests in southern New Brunswick, Canada. Journal of Applied Phycology, 23, 401-407.
[20]	Cubit, J. D. (1984). Herbivory and the seasonal abundance of algae on a high intertidal rocky shore. Ecology, 65, 1904-1917.
[21]	Åberg, P. (1992). Size-based demography of the seaweed Ascophyllum nodosum in stochastic environments. Ecology, 73, 1488-1501.
[22]	Aberg, P. (1992). A demographic study of two populations of the seaweed Ascophyllum nodosum. Ecology, 73, 1473-1487.
[23]	Dudgeon, S., & Petraitis, P. S. (2005). First year demography of the foundation species, Ascophyllum nodosum, and its community implications. Oikos, 109, 405-415.
[24]	Mathieson, A. C., Penniman, C. A., Busse, P. K., & Tveter-Gallagher, E. (1982). Effects Of Ice On Ascophyllum Nodosum Within The Great Bay Estuary System Of New Hampshire-Maine. Journal of Phycology, 18, 331-336.
[25]	Jenkins, S. R., Norton, T., & Hawkins, S. J. (2004). Long term effects of Ascophyllum nodosum canopy removal on mid shore community structure. Journal of the Marine Biological Association of the UK, 84, 327-329.
[26]	McCook, L. J., & Chapman, A. R. O. (1997). Patterns and variations in natural succession following massive ice-scour of a rocky intertidal seashore. Journal of Experimental Marine Biology and Ecology, 214, 121-147.
[27]	Olsen, J. L., Zechman, F. W., Hoarau, G., Coyer, J. A., Stam, W. T., Valero, M., & Åberg, P. (2010). The phylogeographic architecture of the fucoid seaweed Ascophyllum nodosum: an intertidal ‘marine tree’and survivor of more than one glacial–interglacial cycle. Journal of Biogeography, 37, 842-856.
[28]	Toth, G. B., & Pavia, H. (2006). Artificial wounding decreases plant biomass and shoot strength of the brown seaweed Ascophyllum nodosum (Fucales, Phaeophyceae). Marine Biology, 148, 1193-1199.
[29]	Pavia, H., Cervin, G., Lindgren, A. & Åberg P. (1997). Effects of UV-B radiation and simulated herbivory on phlorotannins in the brown alga Ascophyllum nodosum. Marine Ecology Progress Series, 157, 139-146.
[30]	Pavia, H., & Toth, G. B. (2000). Inducible chemical resistance to herbivory in the brown seaweed Ascophyllum nodosum. Ecology, 81, 3212-3225.
[31]	Pavia, H., Toth, G., & Åberg, P. (1999). Trade-offs between phlorotannin production and annual growth in natural populations of the brown seaweed Ascophyllum nodosum. Journal of Ecology, 87, 761-771.
[32]	Davies, A. J. & Johnson, M. P. (2006). Coastline configuration disrupts the effects of large-scale climatic forcing, leading to divergent temporal trends in wave exposure. Estuarine Coastal and Shelf Science, 69, 643-648.
[33]	Lindegarth, M. & Gamfeldt, L. (2005). Comparing categorical and continuous ecological analyses: Effects of "wave exposure" on rocky shores. Ecology, 86, 1346-1357.
[34]	Viejo, R. M., & Åberg, P. (2003). Temporal and spatial variation in the density of mobile epifauna and grazing damage on the seaweed Ascophyllum nodosum. Marine Biology, 142, 1229-1241.
[35]	Kurr, M., & Davies, A. J. (2018). Time-since-invasion increases native mesoherbivore feeding rates on the invasive alga, Sargassum muticum (Yendo) Fensholt. Journal of the Marine Biological Association of the United Kingdom, 98, 1935-1944.
[36]	Åberg, P. (1989). Distinguishing between genetic individuals in Ascophyllum nodosum populations on the Swedish west coast. British Phycological Journal, 24, 183-190.
[37]	Åberg, P. (1990). Measuring size and choosing category size for a transition matrix study of the seaweed Ascophyllum nodosum. Marine Ecology Progress Series, 63, 281-287.
[38]	Van Alstyne, K. L. (1995). Comparison of three methods for quantifying brown algal polyphenolic compounds. Journal of Chemical Ecology, 21, 45-58.
[39]	Littler, M. M. & Littler D. S. (eds) (1985). Handbook of Phycological Methods, volume 2-4. Ecological field methods; macroalgae. Cambridge University Press, New York, USA.
[40]	Holme, N. A. & McIntyre, A. D. (1984) Methods for the Study of Marine Benthos. Blackwell Scientific Publications, Oxford, UK.
[41]	Neilson, A. H., & Lewin, R. A. (1974). The uptake and utilization of organic carbon by algae: an essay in comparative biochemistry. Phycologia, 13, 227-264.
[42]	Lamare, M. D., & Wing, S. R. (2001). Calorific content of New Zealand marine macrophytes. New Zealand Journal of Marine and Freshwater Research, 35, 335-341.
[43]	Forrest, R. E., Chapman, M. G., & Underwood, A. J. (2001). Quantification of radular marks as a method for estimating grazing of intertidal gastropods on rocky shores. Journal of Experimental Marine Biology and Ecology, 258, 155-171.
[44]	Connan, S., & Stengel, D. B. (2011). Impacts of ambient salinity and copper on brown algae: 2. Interactive effects on phenolic pool and assessment of metal binding capacity of phlorotannin. Aquatic Toxicology, 104, 1-13.
[45]	Liu, X., Bogaert, K., Engelen, A. H., Leliaert, F., Roleda, M. Y., & De Clerck, O. (2017). Seaweed reproductive biology: environmental and genetic controls. Botanica marina, 60, 89-108.
[46]	Suda, M., & Mikami, K. (2020). Reproductive Responses to Wounding and Heat Stress in Gametophytic Thalli of the Red Alga Pyropia yezoensis. Frontiers in Marine Science, 7, 394.

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Martyn Kurr, Andrew John Davies. (2020). Drivers of Sex-specific Trade-offs in the Macroalga Ascophyllum nodosum. Plant, 8(3), 54-63. https://doi.org/10.11648/j.plant.20200803.12

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Martyn Kurr; Andrew John Davies. Drivers of Sex-specific Trade-offs in the Macroalga Ascophyllum nodosum. Plant. 2020, 8(3), 54-63. doi: 10.11648/j.plant.20200803.12

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AMA Style

Martyn Kurr, Andrew John Davies. Drivers of Sex-specific Trade-offs in the Macroalga Ascophyllum nodosum. Plant. 2020;8(3):54-63. doi: 10.11648/j.plant.20200803.12

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@article{10.11648/j.plant.20200803.12,
  author = {Martyn Kurr and Andrew John Davies},
  title = {Drivers of Sex-specific Trade-offs in the Macroalga Ascophyllum nodosum},
  journal = {Plant},
  volume = {8},
  number = {3},
  pages = {54-63},
  doi = {10.11648/j.plant.20200803.12},
  url = {https://doi.org/10.11648/j.plant.20200803.12},
  eprint = {https://article.sciencepublishinggroup.com/pdf/10.11648.j.plant.20200803.12},
  abstract = {Little is known about reproductive trade-offs in seaweeds, but sex-specific differences in mortality, production of metabolites, threshold size for reproduction, and susceptibility to herbivory have been reported. The macroalga Ascophyllum nodosum exhibits sex-specific trade-offs at sites where wave-action and herbivory are stronger, because females increase their investment into reproduction at the expense of chemical defences. Females may do this at stressed sites because of high germling and juvenile mortality, or to compensate for lower fecundity due smaller adult sizes at these sites. This study aimed to determine which is the case by comparing A. nodosum in an area where stressors (wave-action and herbivory) impacted upon both adult performance and juvenile mortality, to one where only adult performance was impacted (by ice-damage). Seven populations of the algae were compared at both the regional (> 1000 km) and local scales (A. nodosum are caused by some stressors, not caused by others, and are present in some fashion regardless of stress. This is the first study to directly quantify sex-specific trade-offs at different spatial scales in populations of either plants or algae, and as such it reveals novel insights into the driving forces behind them.},
 year = {2020}
}

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TY  - JOUR
T1  - Drivers of Sex-specific Trade-offs in the Macroalga Ascophyllum nodosum
AU  - Martyn Kurr
AU  - Andrew John Davies
Y1  - 2020/09/03
PY  - 2020
N1  - https://doi.org/10.11648/j.plant.20200803.12
DO  - 10.11648/j.plant.20200803.12
T2  - Plant
JF  - Plant
JO  - Plant
SP  - 54
EP  - 63
PB  - Science Publishing Group
SN  - 2331-0677
UR  - https://doi.org/10.11648/j.plant.20200803.12
AB  - Little is known about reproductive trade-offs in seaweeds, but sex-specific differences in mortality, production of metabolites, threshold size for reproduction, and susceptibility to herbivory have been reported. The macroalga Ascophyllum nodosum exhibits sex-specific trade-offs at sites where wave-action and herbivory are stronger, because females increase their investment into reproduction at the expense of chemical defences. Females may do this at stressed sites because of high germling and juvenile mortality, or to compensate for lower fecundity due smaller adult sizes at these sites. This study aimed to determine which is the case by comparing A. nodosum in an area where stressors (wave-action and herbivory) impacted upon both adult performance and juvenile mortality, to one where only adult performance was impacted (by ice-damage). Seven populations of the algae were compared at both the regional (> 1000 km) and local scales (A. nodosum are caused by some stressors, not caused by others, and are present in some fashion regardless of stress. This is the first study to directly quantify sex-specific trade-offs at different spatial scales in populations of either plants or algae, and as such it reveals novel insights into the driving forces behind them.
VL  - 8
IS  - 3
ER  -

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Author Information

Martyn Kurr

School of Ocean Sciences, Bangor University, Menai Bridge, the United Kingdom
Andrew John Davies

Department of Biological Sciences, University of Rhode Island, Kingston, the United States

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Martyn Kurr, Andrew John Davies. (2020). Drivers of Sex-specific Trade-offs in the Macroalga Ascophyllum nodosum. Plant, 8(3), 54-63. https://doi.org/10.11648/j.plant.20200803.12

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ACS Style

Martyn Kurr; Andrew John Davies. Drivers of Sex-specific Trade-offs in the Macroalga Ascophyllum nodosum. Plant. 2020, 8(3), 54-63. doi: 10.11648/j.plant.20200803.12

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AMA Style

Martyn Kurr, Andrew John Davies. Drivers of Sex-specific Trade-offs in the Macroalga Ascophyllum nodosum. Plant. 2020;8(3):54-63. doi: 10.11648/j.plant.20200803.12

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@article{10.11648/j.plant.20200803.12,
  author = {Martyn Kurr and Andrew John Davies},
  title = {Drivers of Sex-specific Trade-offs in the Macroalga Ascophyllum nodosum},
  journal = {Plant},
  volume = {8},
  number = {3},
  pages = {54-63},
  doi = {10.11648/j.plant.20200803.12},
  url = {https://doi.org/10.11648/j.plant.20200803.12},
  eprint = {https://article.sciencepublishinggroup.com/pdf/10.11648.j.plant.20200803.12},
  abstract = {Little is known about reproductive trade-offs in seaweeds, but sex-specific differences in mortality, production of metabolites, threshold size for reproduction, and susceptibility to herbivory have been reported. The macroalga Ascophyllum nodosum exhibits sex-specific trade-offs at sites where wave-action and herbivory are stronger, because females increase their investment into reproduction at the expense of chemical defences. Females may do this at stressed sites because of high germling and juvenile mortality, or to compensate for lower fecundity due smaller adult sizes at these sites. This study aimed to determine which is the case by comparing A. nodosum in an area where stressors (wave-action and herbivory) impacted upon both adult performance and juvenile mortality, to one where only adult performance was impacted (by ice-damage). Seven populations of the algae were compared at both the regional (> 1000 km) and local scales (A. nodosum are caused by some stressors, not caused by others, and are present in some fashion regardless of stress. This is the first study to directly quantify sex-specific trade-offs at different spatial scales in populations of either plants or algae, and as such it reveals novel insights into the driving forces behind them.},
 year = {2020}
}

Copy | Download

TY  - JOUR
T1  - Drivers of Sex-specific Trade-offs in the Macroalga Ascophyllum nodosum
AU  - Martyn Kurr
AU  - Andrew John Davies
Y1  - 2020/09/03
PY  - 2020
N1  - https://doi.org/10.11648/j.plant.20200803.12
DO  - 10.11648/j.plant.20200803.12
T2  - Plant
JF  - Plant
JO  - Plant
SP  - 54
EP  - 63
PB  - Science Publishing Group
SN  - 2331-0677
UR  - https://doi.org/10.11648/j.plant.20200803.12
AB  - Little is known about reproductive trade-offs in seaweeds, but sex-specific differences in mortality, production of metabolites, threshold size for reproduction, and susceptibility to herbivory have been reported. The macroalga Ascophyllum nodosum exhibits sex-specific trade-offs at sites where wave-action and herbivory are stronger, because females increase their investment into reproduction at the expense of chemical defences. Females may do this at stressed sites because of high germling and juvenile mortality, or to compensate for lower fecundity due smaller adult sizes at these sites. This study aimed to determine which is the case by comparing A. nodosum in an area where stressors (wave-action and herbivory) impacted upon both adult performance and juvenile mortality, to one where only adult performance was impacted (by ice-damage). Seven populations of the algae were compared at both the regional (> 1000 km) and local scales (A. nodosum are caused by some stressors, not caused by others, and are present in some fashion regardless of stress. This is the first study to directly quantify sex-specific trade-offs at different spatial scales in populations of either plants or algae, and as such it reveals novel insights into the driving forces behind them.
VL  - 8
IS  - 3
ER  -

Copy | Download