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Who Cares More about Chemical Defenses — the Macroalgal Producer or Its Main Grazer?

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Abstract

The consequences of defensive secondary metabolite concentrations and interspecific metabolite diversity on grazers have been extensively investigated. Grazers which prefer certain food sources are often found in high abundance on their host and as a result, understanding the interaction between the two is important to understand community structure. The effects of intraspecific diversity, however, on the grazer are not well understood. Within a single, localized geographic area, the Antarctic red seaweed Plocamium sp. produces 15 quantitatively and qualitatively distinct mixtures of halogenated monoterpenes (“chemogroups”). Plocamium sp. is strongly chemically defended which makes it unpalatable to most grazers, except for the amphipod Paradexamine fissicauda. We investigated differences in the feeding and growth rates of both Plocamium sp. and P. fissicauda, in addition to grazer reproductive output, in relation to different chemogroups. Some chemogroups significantly reduced the grazer’s feeding rate compared to other chemogroups and a non-chemically defended control. The growth rate of Plocamium sp. did not differ between chemogroups and the growth rates of P. fissicauda also did not show clear patterns between the feeding treatments. Reproductive output, however, was significantly reduced for amphipods on a diet of algae possessing one of the chemogroups when compared to a non-chemically defended control. Hence, intraspecific chemodiversity benefits the producer since certain chemogroups are consumed at a slower rate and the grazer’s reproductive output is reduced. Nevertheless, the benefits outweigh the costs to the grazer as it can still feed on its host and closely associates with the alga for protection from predation.

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REFERENCES

  • Adler F, Karban R (1994) Defended fortresses or moving targets? Another model of inducible defenses inspired by military metaphors. Am Nat 144:813–832. https://doi.org/10.1086/285708

  • Agrawal AA, Hastings AP, Johnson MTJ, et al (2012) Insect herbivores drive real-time ecological and evolutionary change in plant populations. Science 338:113–116. https://doi.org/10.1126/science.1225977

  • Agrawal AA, Böröczky K, Haribal M, et al (2021) Cardenolides, toxicity, and the costs of sequestration in the coevolutionary interaction between monarchs and milkweeds. Proc Natl Acad Sci U. S. A. 118:1–8. https://doi.org/10.1073/pnas.2024463118

  • Amsler CD, Rowley RJ, Laur DR, et al (1995) Vertical distribution of Antarctic peninsular macroalgae: cover, biomass, and species composition. Phycologia 34:424–430. https://doi.org/10.2216/i0031-8884-34-5-424.1

  • Amsler CD, Iken K, McClintock J.B., et al (2005) Comprehensive evaluation of the palatability and chemical defenses of subtidal macroalgae from the Antarctic Peninsula. Mar Ecol Prog Ser 294:141–159. https://doi.org/10.3354/meps294141

  • Amsler CD, McClintock JB, Baker BJ (2008) Macroalgal chemical defenses in polar marine communities. In: Amsler CD (ed) Algal chemical ecology. Springer, Berlin, pp 91–103. https://doi.org/10.1007/978-3-540-74181-7_4

  • Amsler CD, Iken K, McClintock JB, Baker BJ (2009) Defenses of polar macroalgae against herbivores and biofoulers. Bot Mar 52:535–545. https://doi.org/10.1515/BOT.2009.070

  • Amsler CD, McClintock JB, Baker BJ (2012a) Palatability of living and dead detached Antarctic macroalgae to consumers. Antarct Sci 24:589–590. https://doi.org/10.1017/S0954102012000624

  • Amsler CD, McClintock JB, Baker BJ (2012b) Amphipods exclude filamentous algae from the Western Antarctic Peninsula benthos: experimental evidence. Polar Biol 35:171–177. https://doi.org/10.1007/s00300-011-1049-3

  • Amsler CD, McClintock JB, Baker BJ (2014) Chemical mediation of mutualistic interactions between macroalgae and mesograzers structure unique coastal communities along the western Antarctic Peninsula. J Phycol 50:1–10. https://doi.org/10.1111/jpy.12137

    Article  PubMed  Google Scholar 

  • Amsler CD, Amsler MO, Curtis MD, et al (2019) Impacts of gastropods on epiphytic microalgae on the brown macroalga Himantothallus grandifolius. Antarct Sci 31:89–97. https://doi.org/10.1017/S0954102019000014

  • Amsler CD, McClintock JB, Baker BJ (2020) Chemical mediation of Antarctic macroalga-grazer interactions. In: Gómez I, Huovinen P (eds) Antarctic seaweeds. Springer, Cham. pp 339–363. https://doi.org/10.1007/978-3-030-39448-6_17

  • Amsler MO, Amsler CD, von Salm JL, et al (2013) Tolerance and sequestration of macroalgal chemical defenses by an Antarctic amphipod: a “cheater” among mutualists. Mar Ecol Prog Ser 490:79–90. https://doi.org/10.3354/meps10446

  • Amsler MO, Huang YM, Engl W, et al (2015) Abundance and diversity of gastropods associated with dominant subtidal macroalgae from the western Antarctic Peninsula. Polar Biol 38:1171–1181. https://doi.org/10.1007/s00300-015-1681-4

  • Ankisetty S, Nandiraju S, Win H, et al (2004) Chemical investigation of predator-deterred macroalgae from the Antarctic Peninsula. J Nat Prod 67:1295–1302. https://doi.org/10.1021/np049965c

  • Anstett DN, Cheval I, D’Souza C, et al (2019) Ellagitannins from the Onagraceae decrease the performance of generalist and specialist herbivores. J Chem Ecol 45:86–94. https://doi.org/10.1007/s10886-018-1038-x

  • Aumack CF, Amsler CD, McClintock JB, Baker BJ (2010) Chemically mediated resistance to mesoherbivory in finely branched macroalgae along the western Antarctic Peninsula. Eur J Phycol 45:19–26. https://doi.org/10.1080/09670260903171668

  • Aumack CF, Amsler CD, McClintock JB, Baker BJ (2011) Impacts of mesograzers on epiphyte and endophyte growth associated with chemically defended macroalgae from the western Antarctic Peninsula: a mesocosm experiment. J Phycol 47:36–41. https://doi.org/10.1111/j.1529-8817.2010.00927.x

  • Aumack CF, Lowe AT, Amsler CD, et al (2017) Gut content, fatty acid, and stable isotope analyses reveal dietary sources of macroalgal-associated amphipods along the western Antarctic Peninsula. Polar Biol 40:1371–1384. https://doi.org/10.1007/s00300-016-2061-4

  • Avila C, Taboada S, Núñez-Pons L (2008) Antarctic marine chemical ecology: what is next? Mar Ecol 29:1–71. https://doi.org/10.1111/j.1439-0485.2007.00215.x

  • Baldwin IT (1998) Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proc Natl Acad Sci U. S. A. 95:8113–8118. https://doi.org/10.1073/pnas.95.14.8113

  • Becerra JX (2007) The impact of herbivore-plant coevolution on plant community structure. Proc Natl Acad Sci U. S. A. 104:7483–7488. https://doi.org/10.1073/pnas.0608253104

  • Berenbaum M, Feeny P (1981) Toxicity of angular furanocoumarins to swallowtail butterflies: escalation in a coevolutionary arms race? Science 212:927–929. https://www.science.org/doi/https://doi.org/10.1126/science.212.4497.927

  • Böttger A, Vothknecht U, Bolle C, Wolf A (2018) Plant secondary metabolites and their general function in plants. In: Böttger A, Vothknecht U, Bolle C, Wolf A (eds) Lessons on caffeine, Cannabis & Co. Learning materials in biosciences. Springer, Cham, pp 3–17. https://doi.org/10.1007/978-3-319-99546-5_1

  • Breier CF, Buskey EJ (2007) Effects of the red tide dinoflagellate, Karenia brevis, on grazing and fecundity in the copepod Acartia tonsa. J Plankton Res 29:115–126. https://doi.org/10.1093/plankt/fbl075

  • Brouwer PEM, Geilen EFM, Gremmen NJM, Lent F (1995) Biomass, cover and zonation pattern of sublittoral macroalgae at Signy Island, South Orkney Islands, Antarctica. Bot Mar 38:259–270. https://doi.org/10.1515/botm.1995.38.1-6.259

  • Bugni TS, Singh MP, Chen L, et al (2004) Kalihinols from two Acanthella cavernosa sponges: inhibitors of bacterial folate biosynthesis. Tetrahedron 60:6981–6988. https://doi.org/10.1016/j.tet.2003.08.082

  • Cabin RJ, Mitchell RJ (2000) To Bonferroni or not to Bonferroni: when and how are the questions. Bull Ecol Soc Am 81:246–248

    Google Scholar 

  • Castañeda LE, Figueroa CC, Fuentes-Contreras E, et al (2009) Energetic costs of detoxification systems in herbivores feeding on chemically defended host plants: a correlational study in the grain aphid, Sitobion avenae. J Exp Biol 212:1185–1190. https://doi.org/10.1242/jeb.020990

  • Cipollini D, Walters D, Voelckel C (2017) Costs of resistance in plants: from theory to evidence. Ann Plant Rev 47:263–307. https://doi.org/10.1002/9781119312994.apr0512

  • Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edition. Lawrence Erlbaum Associates, New York. https://doi.org/10.4324/9780203771587

  • Cruz-Rivera E, Hay ME (2003) Prey nutritional quality interacts with chemical defenses to affect consumer feeding and fitness. Ecol Monogr 73:483–506. https://doi.org/10.1890/0012-9615(2003)073[0483:PNQIWC]2.0.CO;2

  • Dworjanyn SA, Wright JT, Paul NA, et al (2006) Cost of chemical defence in the red alga Delisea pulchra. Oikos 113:13–22. https://doi.org/10.1111/j.0030-1299.2006.14359.x

  • Ehrlich PR, Raven PH (1964) Butterflies and plants: a study in coevolution. Evolution 18:586–608. https://doi.org/10.1111/j.1558-5646.1964.tb01674.x

  • Garamszegi LZ (2006) Comparing effect sizes across variables: generalization without the need for Bonferroni correction. Behav Ecol 17:682–687. https://doi.org/10.1093/beheco/ark005

  • Gerwick W, Fenical W (1981) Ichthyotoxic and cytotoxic metabolites of the tropical brown alga Stypopodium zonale (Lamouroux) Papenfuss. J Org Chem 46:22–27. https://doi.org/10.1021/jo00314a005

  • Gutbrodt B, Dorn S, Unsicker SB, Mody K (2012) Species-specific responses of herbivores to within-plant and environmentally mediated between-plant variability in plant chemistry. Chemoecology 22:101–111. https://doi.org/10.1007/s00049-012-0102-1

  • Hahn PG, Keefover-Ring K, Nguyen LM, Maron JL (2021) Intraspecific correlations between growth and defence vary with resource availability and differ within and among populations. Func Ecol 1–10. https://doi.org/10.1111/1365-2435.13878

  • Harborne JB (1993) Introduction to ecological biochemistry, 4th edition. Academic Press Limited

  • Hay ME (1984) Predictable spatial escapes from herbivory: how do these affect the evolution of herbivore resistance in tropical marine communities? Oecologia 64:396–407. https://doi.org/10.1007/BF00379139

  • Hay ME, Fenical W (1988) Marine plant-herbivore interactions: the ecology of chemical defense. Annu Rev Ecol Syst 19:111–145. https://doi.org/10.1146/annurev.ecolsys.19.1.111

  • Hay ME, Steinberg P (1992) The chemical ecology of plant-herbivore interactions in marine versus terrestrial communities. In: Rosenthal J, Berenbaum M (eds) Herbivores: their interaction with secondary metabolites – vol 2: evolutionary and ecological processes. Academic Press, San Diego, pp 371–413. https://doi.org/10.1016/B978-0-08-092545-5.50015-8

  • Heiser S, Amsler CD, McClintock JB, et al (2020) Every rule has an exception: a cheater in the community-wide mutualism in Antarctic seaweed forests. Integr Comp Biol 60:1358–1368. https://doi.org/10.1093/icb/icaa058

  • Hope RM (2013) Rmisc: Rmisc: Ryan miscellaneous. R package version 1.5. https://www.CRAN.R-project.org/package=Rmisc

  • Hothorn T, Hornik K, van de Wiel MA, Zeileis A (2008) Implementing a class of permutation tests: the coin package. J Stat Softw 28:1–23. https://doi.org/10.18637/jss.v028.i08

  • Huang YM, Amsler MO, McClintock JB, et al (2007) Patterns of gammaridean amphipod abundance and species composition associated with dominant subtidal macroalgae from the western Antarctic Peninsula. Polar Biol 30:1417–1430. https://doi.org/10.1007/s00300-007-0303-1

  • Huntley M, Sykes P, Rohan S, Marin V (1986) Chemically-mediated rejection of dinoflagellate prey by the copepods Calanus pacificus and Paracalanus parvus: mechanism, occurrence and significance. Mar Ecol Prog Ser 28:105–120. https://doi.org/10.3354/meps028105

  • Janzen DH (1980) When is it coevolution? Evolution 34:611–612. https://doi.org/10.1111/j.1558-5646.1980.tb04849.x

  • Kassambara A (2021) rstatix: pipe-friendly framework for basic statistical tests. R package version 0.7.0. https://www.CRAN.R-project.org/package=rstatix

  • Koricheva J (2002) Meta-analysis of sources of variation in fitness costs of plant antiherbivore defenses. Ecology 83:176–190. https://doi.org/10.1890/0012-9658(2002)083[0176:MAOSOV]2.0.CO;2

  • Macel M, Klinkhamer PGL, Vrieling K, van der Meijden E (2002) Diversity of pyrrolizidine alkaloids in Senecio species does not affect the specialist herbivore Tyria jacobaeae. Oecologia 133:541–550. https://doi.org/10.1007/s00442-002-1074-6

  • Marques LV, Villaça R, Pereira RC (2006) Susceptibility of macroalgae to herbivorous fishes at Rocas Atoll, Brazil. Bot Mar 49:379–385. https://doi.org/10.1515/bot.2006.049

  • Moon B, Park YC, McClintock JB, Baker BJ (2000) Structure and bioactivity of erebusinone, a pigment from the Antarctic sponge Isodictya erinacea. Tetrahedron 56:9057–9062. https://doi.org/10.1016/s0040-4020(00)00760-2

  • Moore BD, Andrew RL, Külheim C, Foley WJ (2014) Explaining intraspecific diversity in plant secondary metabolites in an ecological context. New Phytol 201:733–750. https://doi.org/10.1111/nph.12526

  • Moran MD (2003) Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 100:403–405. https://doi.org/10.1034/j.1600-0706.2003.12010.x

  • Mutikainen P, Walls M, Ovaska J, et al (2002) Costs of herbivore resistance in clonal saplings of Betula pendula. Oecologia 133:364–371. https://doi.org/10.1007/s00442-002-1021-6

  • Nakagawa S (2004) A farewell to Bonferroni: the problems of low statistical power and publication bias. Behav Ecol 15:1044–1045. https://doi.org/10.1093/beheco/arh107

  • de Nys R, Coll JC, Bowden BF (1992) Delisea pulchra (cf. fimbriata) revisited. The structural determination of two new metabolites from the red alga Delisea pulchra. Aust J Chem 45:1625–1632. https://doi.org/10.1071/CH9921625

  • de Nys R, Wright AD, König GM, Sticher O (1993) New halogenated furanones from the marine alga Delisea pulchra (cf. fimbriata). Tetrahedron 49:11213–11220. https://doi.org/10.1016/S0040-4020(01)81808-1

  • Paul V, Fenical W (1986) Chemical defense in tropical green algae, order Caulerpales. Mar Ecol Prog Ser 34:157–169. https://doi.org/10.3354/meps034157

  • Paul VJ, Arthur KE, Ritson-Williams R, et al (2007) Chemical defenses: from compounds to communities. Biol Bull 213:226–251. https://doi.org/10.2307/25066642

  • Pesando D, Lemée R, Ferrua C, et al (1996) Effects of caulerpenyne, the major toxin from Caulerpa taxifolia on mechanisms related to sea urchin egg cleavage. Aquat Toxicol 35:139–155. https://doi.org/10.1016/0166-445X(96)00013-6

  • Peters KJ, Amsler CD, Amsler MO, et al (2005) A comparative analysis of the nutritional and elemental composition of macroalgae from the western Antarctic Peninsula. Phycologia 44:453–463. https://doi.org/10.2216/0031-8884(2005)44[453:ACAOTN]2.0.CO;2

  • Provasoli L (1968) Media and prospects for the cultivation of marine algae. In: Watanabe A, Hattori A (eds) Cultures and collections of algae, Proc. U.S.-Japan Conf. Hakone, September 1966. Japanese Society of Plant Physiologists, pp 63–75

  • Rasher DB, Stout EP, Engel S, Shearer T, Kubanek J, Hay ME (2015) Marine and terrestrial herbivores display convergent chemical ecology despite 400 million years of independent evolution. Proc Natl Acad Sci U. S. A. 112:12110–12115. https://doi.org/10.1073/pnas.1508133112

  • Reichardt W, Dieckmann G (1985) Kinetics and trophic role of bacterial degradation of macro-algae in Antarctic coastal waters. In: Siegfried WR, Condy P, Laws RM (eds). Springer-Verlag, Berlin, pp 115–122. https://doi.org/10.1007/978-3-642-82275-9_17

  • Rothman KJ (1990) No adjustments are needed for multiple comparisons. Epidemiology 1:43–46. https://doi.org/10.1097/00001648-199001000-00010

  • Rovirosa J, Soler A, Blanc V, Leon R, San-Martin A (2013) Bioactive monoterpenes from Antarctic Plocamium cartilagineum. J Chil Chem Soc 58: 225–226. http://dx.doi.org/https://doi.org/10.4067/S0717-97072013000400026

  • Sampedro L, Moreira X, Zas R (2011) Costs of constitutive and herbivore-induced chemical defences in pine trees emerge only under low nutrient availability. J Ecol 99:818–827. https://doi.org/10.1111/j.1365-2745.2011.01814.x

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. https://doi.org/10.1038/nmeth.2089

  • Shilling AJ, von Salm JL, Sanchez AR, et al (2019) Anverenes B–E, new polyhalogenated monoterpenes from the Antarctic red alga Plocamium cartilagineum. Mar Drugs 17:230. https://doi.org/10.3390/md17040230

  • Shilling AJ, Heiser S, Amsler CD, et al (2021) Hidden diversity in an Antarctic algal forest: metabolomic profiling linked to patterns of genetic diversification in the Antarctic red alga Plocamium sp. Mar Drugs 19:1–13. https://doi.org/10.3390/md19110607

  • Sotka EE, Hay ME (2002) Geographic variation among herbivore populations in tolerance for a chemically rich seaweed. Ecology 83:2721–2735. https://doi.org/10.1890/0012-9658(2002)083[2721:GVAHPI]2.0.CO;2

  • Sotka EE, Reynolds PL (2011) Rapid experimental shift in host use traits of a polyphagous marine herbivore reveals fitness costs on alternative hosts. Evol Ecol 25:1335–1355. https://doi.org/10.1007/s10682-011-9473-y

  • Sotka EE, Whalen KE (2008) Herbivore offense in the sea: the detoxification and transport of secondary metabolites. In: Amsler C (eds) Algal chemical ecology, 1st Edition. Springer, Berlin, pp 203–228. https://doi.org/10.1007/978-3-540-74181-7_10

  • Sotka EE, Jormalainen V, Poore AGB (2018) The evolution of marine herbivores in response to algal secondary metabolites. In: Puglisi MP, Becerro MA (eds) Chemical ecology, 1st Edition. CRC Press, Boca Raton, pp 193–220. https://doi.org/10.1201/9780429453465

  • Steinberg PD (1995) Seasonal variation in the relationship between growth rate and phlorotannin production in the kelp Ecklonia radiata. Oecologia 102:169–173. https://doi.org/10.1007/BF00333248

  • Stierle DB, Sims JJ (1979) Polyhalogenated cyclic monoterpenes from the red alga Plocamium cartilagineum of Antarctica. Tetrahedron 35:1261–1265. https://doi.org/10.1016/0040-4020(79)80051-4

  • Stierle DB, Wing RM, Sims JJ (1979) Polyhalogenated acyclic monoterpenes from the red alga Plocamium of Antarctica. Tetrahedron 35:2855–2859. https://doi.org/10.1016/S0040-4020(01)99499-2

  • Stowe KA, Marquis RJ (2011) Costs of defense: correlated responses to divergent selection for foliar glucosinolate content in Brassica rapa. Evol Ecol 25:763–775. https://doi.org/10.1007/s10682-010-9443-9

  • Taylor RB, Lindquist N, Kubanek J, Hay ME (2003) Intraspecific variation in palatability and defensive chemistry of brown seaweeds: effects on herbivore fitness. Oecologia 136:412–423. https://doi.org/10.1007/s00442-003-1280-x

  • R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.

    Google Scholar 

  • Thackray DJ, Wrattent SD, Edwards PJ, Niemeyer HM (1990) Resistance to the aphids Sitobion avenae and Rhopalosiphum padi in Gramineae in relation to hydroxamic acid levels. Ann Appl Biol 116:573–582. https://doi.org/10.1111/j.1744-7348.1990.tb06640.x

  • Thiel T, Gaschler S, Mody K, et al (2020) Impact of plant defense level variability on specialist and generalist herbivores. Theor Ecol 13:409–424. https://doi.org/10.1007/s12080-020-00461-y

  • Thurston MH (1972) The crustacea amphipoda of Signy Island, South Orkney Islands. British Antarctic Survey Report 71:1–133.

  • Tomczak M, Tomczak E (2014) The need to report effect size estimates revisited. An overview of some recommended measures of effect size. Trends Sport Sci 1:19–25

    Google Scholar 

  • Toth GB, Langhamer O, Pavia H (2005) Inducible and constitutive defenses of valuable seaweed tissues: consequences for herbivore fitness. Ecology 86:612–618. https://doi.org/10.1890/04-0484

  • Vergés A, Paul NA, Steinberg PD (2008) Sex and life-history stage alter herbivore responses to a chemically defended red alga. Ecology 89:1334–1343. https://doi.org/10.1890/07-0248.1

  • Whitham TG, Bailey JK, Schweitzer JA, et al (2006) A framework for community and ecosystem genetics: from genes to ecosystems. Nat Rev Genet 7:510–523. https://doi.org/10.1038/nrg1877

  • Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York

    Book  Google Scholar 

  • Wiencke C, Amsler CD (2012) Seaweeds and their communities in polar regions. In: Wiencke C, Bischof K (eds) Seaweed biology: novel insights into ecophysiology, ecology and Utilization. Springer-Verlag, Berlin, pp 265–294. https://doi.org/10.1007/978-3-642-28451-9_13

  • Wiencke C, Amsler CD, Clayton MN (2014) Macroalgae. In: Koubbi P, Griffiths HJ, Raymond B, et al. (eds). Biogeographic Atlas of the Southern Ocean. Cambridge, UK: Scientific Committee on Antarctic Research, pp 66–73.

  • Wright JT, de Nys R, Steinberg PD (2000) Geographic variation in halogenated furanones from the red alga Delisea pulchra and associated herbivores and epiphytes. Mar Ecol Prog Ser 207:227–241. https://doi.org/10.3354/meps207227

  • Wright JT, de Nys R, Poore AGB, Steinberg PD (2004) Chemical defense in a marine alga: heritability and the potential for selection by herbivores. Ecology 85:2946–2959. https://doi.org/10.1890/03-4041

  • Young RM, von Salm JL, Amsler MO, et al (2013) Site-specific variability in the chemical diversity of the Antarctic red alga Plocamium cartilagineum. Marine Drugs 11:2126–2139. https://doi.org/10.3390/md11062126

  • Zamzow JP, Amsler CD, McClintock JB, Baker BJ (2010) Habitat choice and predator avoidance by Antarctic amphipods: the roles of algal chemistry and morphology. Mar Ecol Prog Ser 400:155–163. https://doi.org/10.3354/meps08399

  • Züst T, Heichinger C, Grossniklaus U et al (2012) Natural enemies drive geographic variation in plant defenses. Science 338:116–119. https://doi.org/10.1126/science.1226397

    Article  CAS  PubMed  Google Scholar 

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ACKNOWLEDGMENTS

We extend our deepest thanks the Palmer Station staff from Antarctic Support Contract without whom our field research would not be possible. We are also grateful to M.D. Shilling and K. Smith for tireless assistance in the field and to C.R. Hadfield for assistance constructing experimental chambers. We thank S.A. Krueger-Hadfield, J.M. Lopez-Bautista, and anonymous reviewers for their comments on the manuscript which significantly improved it.

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The authors declare no conflict of interest.

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This research was made possible with the National Science Foundation awards PLR-1341333 (C.D.A. and J.B.M.) and PLR-1341339 (B.J.B.) from the Antarctic Organisms and Ecosystems Program. J.B.M. acknowledges the support of an Endowed University Professorship in Polar and Marine Biology provided by the University of Alabama at Birmingham.

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  1. Department of Biology, University of Alabama at Birmingham, 1300 University Blvd, Birmingham, AL, 35233, USA

    Sabrina Heiser, Charles D. Amsler, Margaret O. Amsler, Lauren Bozarth, Carmen B. Davis & James B. McClintock

  2. Department of Biology, Walla Walla University, 204 S. College Ave, College Place, WA, 99324, USA

    Cecilia J. Brothers

  3. Department of Chemistry, University of South Florida, 4202 E. Fowler Ave, Tampa, FL, 33620, USA

    Andrew J. Shilling & Bill J. Baker

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Heiser, S., Amsler, C.D., Brothers, C.J. et al. Who Cares More about Chemical Defenses — the Macroalgal Producer or Its Main Grazer?. J Chem Ecol 48, 416–430 (2022). https://doi.org/10.1007/s10886-022-01358-2

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  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-022-01358-2

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