Abstract
With few exceptions, the evolutionary consequences of harmful algae to grazers in aquatic systems remain unexplored. To examine both the ecological and evolutionary consequences of harmful algae on marine zooplankton, we used a two-fold approach. In the first approach, we examined the life history responses of two geographically separate Acartia hudsonica (Copepoda Calanoida) populations reared on diets containing the toxic dinoflagellate Alexandrium fundyense . One copepod population was from a region, Casco Bay, Maine, USA, that has experienced recurrent blooms of highly toxic Alexandrium spp. for decades; whereas the other population from Great Bay, New Jersey, USA, has never been exposed to toxic Alexandrium blooms. The life history experiment demonstrated that when the copepod population from New Jersey was reared on a diet containing toxic A. fundyense it exhibited lower somatic growth, size at maturity, egg production and survival than the same population reared on a diet without toxic A. fundyense . In contrast, toxic A. fundyense did not affect the life-history traits of the Maine population. Fitness, finite population growth rate (λ), was significantly reduced in the New Jersey population, but not in the Maine population. These results are consistent with the hypothesis of local adaptation (resistance) of the historically exposed copepod population to the toxic dinoflagellate. In the second approach, we further tested the resistance hypothesis with a laboratory genetic selection experiment with the naïve New Jersey copepod population exposed to a diet containing toxic A. fundyense. This experiment demonstrated that the ingestion and egg production of adult females of naïve copepods fed A. fundyense improved after three generations of being reared on a diet containing the toxic dinoflagellate. The results of the present study have important implications for understanding how grazer populations may respond to the introduction of toxic algae to their environment, and suggest that grazer resistance may be a feedback mechanism that may lead to bloom control.
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References
D.M. Anderson D.M. Kulis G.J. Doucette J.C. Gallagher E. Balech (1994) ArticleTitleBiogeography of toxic dinoflagellates in the genus Alexandrium from the northeastern United States and Canada Mar. Biol. 120 467–478
F. Carlotti S. Nival (1991) ArticleTitleIndividual variability of development in laboratory-reared Temora stylifera copepodites: consequences for the population dynamics and interpretation in the scope of growth and development rules J. Plankton Res. 13 801–813
H. Caswell (1989) Matrix Population Models Sinauer Assoc. Inc. Sunderland, Massachussetts 328
C.C. Caudill A. Bucklin (2004) ArticleTitleMolecular phylogeography and evolutionary history of the estuarine copepod, Acartia tonsa, on the Northwest Atlantic coast Hydrobiology 511 91–102
M.S. Cohn J.B. Mahoney E. Feers (1988) ArticleTitleOccurrence of the dinoflagellate, Gonyaulax tamarensis, in New Jersey Bull. NJ Acad. Sci. 33 45–49
Colin S.P. (2002). Determination and characterization of resistance by populations of the copepod Acartia hudsonica to the toxic dinoflagellate Alexandrium sp. PhD Dissertation.
S.P. Colin H.G. Dam (2002a) ArticleTitleLatitudinal differentiation in the effects of the toxic dinoflagellate Alexandrium spp on the feeding and reproduction of populations of the copepod Acartia hudsonica Harmful Algae 1 113–125
S.P. Colin H.G. Dam (2002b) ArticleTitleTesting for toxic effects of prey on zooplankton using sole versus mixed diets Limnol. Oceanogr. 47 1430–1437 Occurrence Handle10.4319/lo.2002.47.5.1430
S.P. Colin H.G. Dam (2003) ArticleTitleEffects of the toxic dinoflagellate, Alexandrium fundyense, on historically naïve versus exposed populations of the copepod Acartia hudsonica : a test of mechanisms that reduce ingestion rates Mar. Ecol. Prog. Ser. 248 55–65
D.O. Conover E.T. Schultz (1995) ArticleTitlePhenotypic similarity and the evolutionary significance of countergradient variation Trends Ecol. Evol. 10 248–252
T.A. Ebert (1999) Plant and Animal Populations: Methods in Demography Academic Press New York 312
D.S. Falconer (1996) Introduction to Quantitative Genetics Longman London
L.R. Feinberg H.G. Dam (1998) ArticleTitleEffects of diets on dimensions, density and sinking rates of fecal pellets of the copepod Acartia tonsa Mar. Ecol. Prog. Ser. 175 87–96
M. Frangópulos C. Guisande I. Maneiro I. Riveiro J. Franco (2000) ArticleTitleShort-term and long-term effects of the toxic dinoflagellate Alexandrium minutum on the copepod Acartia clausi Mar. Ecol. Prog. Ser. 203 161–169
B.W. Frost (1972) ArticleTitleEffects of size and concentration of food particles on the feeding behavior of the marine planktonic copepod Calanus Pacificus Limnol. Oceanogr. 17 805–815 Occurrence Handle10.4319/lo.1972.17.6.0805
J.J. Gilbert (1990) ArticleTitleDifferential effects of Anabaena affinis on cladocerans and rotifers: mechanisms and implications Ecology 71 1727–1740
R.R.L. Guillard (1975) Culture of phytoplankton for feeding marine invertebrates Smith W.L. Chanley M.H. (Eds) Culture of Marine Animals Plenum Press New York 26–60
N.G. Hairston SuffixJr. W. Lampert C.E. Caceres C.L. Holtmeier L.J. Weider U. Gaedkes J.M. Fischer J.A. Fox D.M. Post (1999) ArticleTitleRapid evolution revealed by dormant eggs Nature 401 446
N.G. Hairston C.L. Holtmeier W. Lampert L.J. Weider D.M. Post J.M. Fischer C.E. Caceras J.A. Fox U. Gaedke (2002) ArticleTitleNatural selection for grazer resistance to toxic cyanobacteria: evolution of phenotypic plasticity? Evolution 55 2203–2214
G.M. Hallegraeff (1993) ArticleTitleA review of harmful algal blooms and their apparent global increase Phycologia 32 79–99
T.J. Hilbish (1996) ArticleTitlePopulation genetics of marine species: the interaction of natural selection and historically differentiated populations J. Exp. Mar. Biol. Ecol. 200 67–83
W.M. Indrasena T.A. Gill (1999) ArticleTitleThermal degradation of paralytic shellfish poisoning toxins in scallop digestive glands Food Res. Int. 32 49–57 Occurrence Handle1:CAS:528:DyaK1MXlsFCht70%3D
P.L. Klerks J.S. Levinton (1989) ArticleTitleRapid evolution of metal resistance in a benthic oligochaete inhabiting a metal-polluted site Biol. Bull. 176 135–141 Occurrence Handle1:CAS:528:DyaL1MXktFyqu70%3D
E.T. Lee (1980) Statistical Methods for Survival Data Analysis Lifetime Learning Publications Belmont, CA
S. Liu Wang W.-X. (2002) ArticleTitleFeeding and reproductive responses of marine copepods in South China to toxic and non-toxic phytoplankton Mar. Biol. 140 595–603
D.J. Lonsdale J.S. Levinton (1985) ArticleTitleLatitudinal differentation in copepod growth: an adaptation to temperature Ecology 66 1397–1407
M.D.G. Lopez (1996) ArticleTitleEffect of starvation on development and survivorship of naupliar Calanus pacificus (Brodsky). J. Exp Mar. Biol. Ecol. 203 133–146
S.N. Luoma (1977) ArticleTitleDetection of trace contaminant effects on aquatic ecosystems J. Fish. Res. Board Can. 34 436–439
J. Mauchline (1998) Advances in Marine Biology: The Biology of Calanoid Copepods NumberInSeries33 Academic Press New York 355
B.J. McAlice (1981) ArticleTitleOn the post-glacial history of Acartia tonsa (Copepoda: Calanoida) in the Gulf of Maine and the Gulf of St Lawrence. Mar. Biol. 64 267–272
Oshima Y., Sugino K. and Yasumoto T. (1989). Latest advances in HPLC analysis of paralytic shellfish toxins. In Mycotoxins and Phycotoxins. Proceedings of the 7th International IUPAC Symposium Natori S. et al., (eds), editors, Amsterdam pp. 319–326.
W.T. Peterson (1986) ArticleTitleDevelopment, growth, and survivorship of the copepod Calanus marshallae in the laboratory Mar. Ecol. Prog. Ser. 29 61–72
D.A. Pyke J.N. Thompson (1986) ArticleTitleStatistical analysis of survival and removal rate experiments Ecology 67 240–245
E.J. Schantz (1986) ArticleTitleChemistry and biology of saxitoxin and related toxins Ann. NY Acad. Sci. 479 15–23 Occurrence Handle1:CAS:528:DyaL2sXhtlejurs%3D Occurrence Handle3468843
T.J. Smayda (1997) ArticleTitleHarmful algal blooms: their ecophysiology and general relevance to phytoplankton blooms in the sea Limnol. Oceanogr. 42 1137 Occurrence Handle10.4319/lo.1997.42.5_part_2.1137
R.R. Sokal F.J. Rohlf (1995) Biometry EditionNumber2 W.H. Freeman San Francisco
C.E. Taylor (1986) ArticleTitleGenetics and evolution of resistance to insecticides Biol. J. Linn. Soc. 27 103–112
G.J. Teegarden A.D. Cembella (1996) ArticleTitleGrazing of toxic dinoflagellates, Alexandrium spp., by adult copepods of coastal Maine: Implications for the fate of paralytic shellfish toxins in marine food webs J. Exp. Mar. Biol. Ecol. 196 145–176
G.J. Teegarden R.G. Campbell E.G. Durbin (2001) ArticleTitleZooplankton feeding behavior and particle selection in natural plankton assemblages containing toxic Alexandrium sp Mar. Ecol. Prog. Ser. 218 213–226
G.J. Teegarden (1999) ArticleTitleCopepod grazing selection and particle discrimination on the basis of PSP toxin content Mar. Ecol. Prog. Ser. 181 163–176 Occurrence Handle1:CAS:528:DC%2BD3cXhs1eqsA%3D%3D
B. Tepper B.P. Bradley (1989) ArticleTitleTemporal changes in a natural population of copepods Biol. Bull. 176 32–40
J. Travis (1996) ArticleTitleThe significance of geographical variation in species interactions Am. Nat. 148 S1–S8
A. Tsuda (1994) ArticleTitleStarvation tolerance of a planktonic marine copepod Pseudocalanus newmani Frost J. Exp. Mar. Biol. Ecol. 181 81–89
Turner J.T., Tester P.A. and Hansen P.J. (1998). Interactions between toxic marine phytoplankton and metazoan and protistan grazers In M.R. Anderson A.D. Ceurbella and G.M. Hallograe (eds) Physiological Ecology of Harmful Algal Blooms, NATO ASI Series, Vol G 41. Springer-Verlag, Berlin, pp 453–474.
H. Utermöhl (1958) ArticleTitleZur vevollkommnung der qualitativen phytoplankton-methodik Mitt Int Theor Agnew Limnol 9 1–38
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Colin, S.P., Dam, H.G. Testing for resistance of pelagic marine copepods to a toxic dinoflagellate. Evol Ecol 18, 355–377 (2005). https://doi.org/10.1007/s10682-004-2369-3
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DOI: https://doi.org/10.1007/s10682-004-2369-3