Chrysophycean Microfossils Provide New Insight into ...

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Chrysophycean Microfossils Provide New lnsight into the Recent History of a Natura y Acidic Lake (Cone Pond, New Hampshire) Katherine N. Gibson and john P. ~ r n o l l Department sf Bio/ogy, Queen's Cniversity, Kingston, One. K76 3N6

and Jesse Ford2 Ecosystems Research Center, C ~ r n e l University, l ithaca, NY 14853, USA

Gibson, K. N., I . P. Smsl, and 1. Ford. 1987. Chrysophycean microfossils provide new insight into the recent history of a naturally acidic lake (Cone Pond, New Hampshire). Can. I. Fish. Aquat. Sci. 44: 1584-

1588. Cone Pond, New Hampshire, is an acidic (pH = 4.5) clearwater lake that is currently fishless. Historical records indicate declining fish populations between 1951 and 1966, but paleoiirnnological work using diatoms failed to find evidence for further recent acidification of this naturally acid site. We initiated new paieoiirnnological studies using mallom~nadaceanchrysophytes to further our understanding of Cone Pond's recent past. Our stratigraphic analyses indicate recent striking changes in the chrysoghyte flora of this lake, with Mallomonas hindonii, a species only common i n recently acidified lakes, replacing M. crassisquama, a cosmopolitan species that dominated the flora over the preceding 8000 yr; this recent change parallels the declines i n fish populations. Because chrysophytes often bloom in early spring and are known, in other lakes, t o experience changes i n community composition before those expressed by the diatom community, a possibility is that chrysophytes track transient excursions of lake water chemistry associated with earsy snowmelt conditions. I n this scenario, chrysophytes would respond to aconstellation of specific short-term chemical changes including, but not restricted to, pH. Such pH associated changes could include changes in concentrations, speciation, or complexation of metals mobilized from the catchment or sediments, all of which are known to affect both chrysophytes and fish. k'etang Cone (New Hampshire) est u n lac d'eau claire acide (pH = 4/51qui est actueHement depouwu d'une fauwe piscicole. Des donnees historiques relgvent un destin des populations de poissons de 1951 B 1966, mais des travaux palCo%imnologiquessur les diatomees n'ont pas revel4 une acidification r4cente additionnelle de cet endroit naturellement acide. kes auteurs ont effectue de nouvelies etudes paleolimnologiques sksr des chrysophycees de la famille Mallomonadaceae afin de rnieux cornprendre le passe recent de l'ktang Cone. Ces analyses stratigraphiques ont rev616 desvariations recentes marquees de la flore chrysophycee de ce lac : Ma!lomonas hindonii, une espece commune seuiement dans les lacs recemment acidifies, a rernplace M. crassisquama, une espece cosmopolite qui a domine la flore au cows des 8 000 ?nnCes precedentes. Ce bouleversernent recent est parall&le au dCclin des populations de poissons. Etant donne que les chsysophycees fleurissent souvent au d4but du printemps et que dans certains lacs, elles subissent des variations de la composition de la communaute avant que les variations de la communaute de diatomees soient exprimees, il se peut que les chrysophycc5es suivent la trace de variations transitoires des facteurs chimiques Iacustres associees i la fonte precoce des neiges. Ainsi, les chrysophycees reagiraient a une conste%lationde variations chirniques prkcises a court terme y compris, mais non exc~usivement,Be pH. De telles variations liees au p H peuvent comprendse des fluctuations de O a concentration, de I1esp&ce ou de la complexation des metaux mobilises du bassin versant au des s6dirnents. O n sait que tous ces facteurs ont une incidence sur les chrysophycees et les poissons. Received February 3, 7987 Accepted May 20, 1987 (J91.22)

ver the Iast decade, a great deal o f scientific attention has k e n focused ow the effects sf acidic precipitation on watershe&%/l&e ecosystems. Although accelerated lake acidification is considered a major factor in the '~uthorto whom co~espndeweeshould be addressed. 2Present address: U.S . Environmental Protection Agency, Cowallis Research Laboratory, 200 Southwest 35th S t ~ e t ,CowaBlis, OW 97333, USA.

disappearance of fish populations, the nature and rates s f change in water chemistry are not weH known. Far these reasons, there has been a great deal of interest in applying paleolimological techniques to provide an historical perspective on processes of lake acidification. Analysis of the stratigraphic distribution of diatom fmstules has been an especially useful technique for inferring past lake conditions, including pH (e.g. Battarbee 1984; Charles and Norton 1986; gapers in Smol et al. %986). More recently, the siliceous scales of md~ownad-


acean chrysophytes have augmented diatom-inferred reconstmceisns sf lake acidification (Smol et al. 1984a, 1984b; Christie and Smol 1986; Smol 1986; Tolonen et al. 1986; Skinberg and Hatmann 1986). Much paleolimological research has centered on the northeastern United States because of the large number of presently acidic and fishless lakes (e.g. Charles 1984; Smsl et al. 1984b; Smol 1986; Charles and Norton 1986). In many of these sites, the paleolimological data showed evidence of recent lake acidification and the authors have suggested that loading of strong acids is the causative factor. In contrast with these findings, a paleolimnological study of the recent history of Cone Pond, a small (4.8 ha) acidic clewater lake in the White Mountains of New Hampshire, yielded no strong evidence of recent acidification (Fig. l), despite circumstantial evidence from fish surveys of recent declines in fish populations (Ford 1986). In 1938, brown bullhead (Pctaiurus nebulosus), chain pickerel (Esox niger) , and yellow perch (Percarnvescens) were present in the pond, but when Cone Pond was treated with rotenone in 1963, only Barge (23-33 cm) yellow perch were found. Subsequent attempts to stock with brook trout (Salvelinusfontinalis) during 1964-68 failed, and the stocking program was cancelled in 1970. Cone Pond is presently fishless, has a pH of 4.5, and has high midsummer total aluminium concentrations (-0.5 mg/L), dthough these vary seasonally with dissolved organic carbon (Buso et d. 1984). Further details about this site are given in Ford (1984, 1986). Ford (1984) demonstrated that Cone Pond is naturally acidic. Its diatom flora shifted from an assemblage dominated by planktonic species (Cyclotella stelligera (Cl. & Grun) V .H . and several species of Melosira) to one dominated by benthic taxa over 7000 yr ago, and virtually all diatom taxa associated with strongly acid conditions were present in the pond by 5000 B.P. (Ford 1984, 1986). Diatom-infed pH reconstructions indicated that the pH of the pond has been K5.0 for at least 1800 yr (Ford 1984). Further paleolimnological studies were needed at Cone Pond to resolve the discrepancies between the historical fisheries record and the paleolimological record with respect to recent anthopgenic acidification. Such ancillary studies are particularly necessary for naturally acidic lakes that would not be expected to exhibit the m a y of rapid biological changes typical of lakes that have only recently had their natural buffering capacity overwhelmed by anthopgenic acidification (e.g . Big Moose Lake, Charles et d . 1987). Mallomonadacean microfossils are ideal candidates to provide such resolution because dlomonadacean chrysophyks persist in the plankton even at low pH and undergo changes in community composition within the pH range 4.5-6.0 (Smsl et al. 1984a, 1984b;Smol1986). In this study, we apply this paleolimnological technique to the Cone Pond sediments. s and Materids The same sediment core and, for most stratigraphic levels, the same slides enumerated in the diatom study (Ford 1986) were used for the chrysophyte analyses. Because both diatom hstules and chrysophycean scales are siliceous, sediment digestions md microscopic techniques are identical for the two groups. Briefly, a piston corer was used to retrieve short sediment cores from near the centre of Cone Pond (Ford 1986). The sediment was extruded and sectioned at l-cm intervals and Can. J . Fish. Aqecdlt. Sci., V s l . 44, 1987

FIG. 1. Diatom-inferred pH history of Cone Pond's recent history (slightly modified from Fsrd '1986). The broken line indicates the cultural horizon. Note that this horizon is '1 cm lower in panel A (core 29 than in panel B (core 1). Profiles of both pollen and loss-on-ignition confirm that these two cores are comparable. Solid circles: Davis and Anderson's ('1985) multiple linear regression based on the first principal component sf the relative frequency of selected diatom bxa in New England surface sediments, low-pH set s f New England lakes; open triangles: Charles' ('1985) multiple linear regression based on a griori assignment of taxa to weighted pH-preference categories.

subsamples were taken for algal microfossils, pollen, loss-onignition, and '''~b dating (Ford 1986). The upper 10 cm was studied at 1-cm intervals, which is finer stratigraphic resolution than that used by Ford's (1986) diatom study. For this section, additional slides were prepared; preparation techniques and counting procedures followed Smol et d . ( 1984a).

Results and Discussion A striking shift in the chrysophyte assemblage begins near 8-9 cm into the core (35-65 yr ago) and levels off at 2 cm (15-30 yr ago; Ford 1986; Fig. 2). Mailomonas crassisquama, (Asmund) Fott, a cosmopolitan taxon that dominated the mallomonadacean assemblage throughout most of the pond's postglacial development (Gibson 1986), sharply declined to trace levels by 5 cm (Fig. 2). This is associated with a striking increase in M. hinalonii Nicholls, which had never been present at greater than trace levels at any time during the Holocene. This species shift is the largest recorded in the pond's 12000-yr history (Gibson 1986). Mallonaoms crassisquama is the most widely distributed of its genus (Cronberg and Kkstiansen 1980; Nicholls 1982), although it rarely thrives in very acidic waters (e.g. Smol et al. 1984a; Smol 1986, and unpubl. data; Steinberg and Hartmann 1986). On the other hand, M. kindonii is the most acidobiontic chrysophyte thus far recorded in North America (Smol et al. 1984a, 1984b; Smol 1986, and unpaabl. data), having an abundance-weighted mean pH sf 4.93 for 47 Adironclack Mountain lakes (D. F. Charles and J. P. Smol, unpubl. data). The species shift in Cone Pond's recent sediments is virtually identical to those recorded in most recently acidified lakes investigated to date. These include lakes in the Adirondack Mountains (Smol et al. 1984b; Smol 1986, and unpubH. data;


CONE POND, N.H. [core 1) FIG. 2. Relative frequency of mallomonadacean scales in the recent sediments of Cone Pond. The data presented here are for core 1; analyses of core 2 provided almost identical results.

Christie and Smol 1986; Charles et al. 1987), Ontario (9. P. Smol and K. Nicholls, unpubl. data), and Europe (Tolonen et al. 1986; Steinberg and Hartmann 1986). In all these studies, chysophyte interpretations reinforced reconstmctions based on diatom assemblages and other paleoindicators. Furthemre, the timing of the chysophyte changes at Cone Pond is similar to that at other recently acidified sites in the northeastern United States (Charles and Norton 1986) and parallels the historically documented decline in fish populations that occurred between 1938 and 1968 at Cone Pond (Ford 1986). During this p e r i d of rapid change in the chysophyte community, only minor fluctuations in diatom species composition occurred (Ford 1986). Both Fragilsria acidsbiontics Charles a d T'abedlaria gusdriseptat~Knudson increased in recent sediments, but these changes were small, and the resulting decline in diatom-inferred pH was subtle and probably not statistically significant (Ford 1986). The diatom flora of Cone Pond had been well-adapted to strongly acid conditions for several thousand years (Ford 1984, 1986). This situation differs from that found in most recently acidified lakes and suggests that by the time anthropogenic acidification began, the diatom community may no longer have had the flexibility to respond to further decreases in lake water pH. For example, loss of planktonic diatom taxa, a characteristic feature of recent anthropogenic lake acidification ( B a t t h e e 1984; Charles B985), occurred at Cone Pond more than 7000 yr ago (Ford 1984). Virtually all alkaliphilous species had been lost and acidobiontic s p i e s gained by 5000 B.P. (Ford 1984, 1986). 'This interpretation of declining lake water pH over the Holocene is consistent with the long-term record of mallomonadacean microfossils ,although the chrysophyte cord suggests more gradual, long-term ecosystem acidification than the diatom and sediment chemistry records (Gibson E 986). The validity of the long-term, diatom-inferred pH rechsnstmctions for Cone Pond is strengthened because (1) two different transfer functions, which were based on different, regionally

appropriate diatom data sets, both accurately predicted the modem pH of Cone Pond (Fig. 11, (2) both transfer functions produced similar historical pH reconstructions, and (3) these reconstructions were consistent with interpretations based on palynology and fractionated geochemical data (Ford 1984, 1986). For these reasons, and because we do not yet have quantitative chrysophyte pH transfer functions, we provisionally choose to accept the general diatom-inferred pH profiles and explore possibilities that complement, rather than contradict, that reconstmction. Mallomonadacean chrysophytes are likely to be more responsive to short-term changes in lake water conditions than benthic diatoms that dominated the postsettlement flora of Cone Pond for several reasons. First, chsysophytes often bloom during the early spring and therefore may be particularly sensitive to short-term changes in water chemistry that occur during snowmelt, The sedimentary diatom assemblage, on the other hand, includes more t a a with a diverse m a y sf ecological chaxacteristics, which tends to integrate over all seasons. Second, mallomonadacean chrysophytes are euplanktonic and continuously bathed in lake water. The benthic diatoms, on the other hand, inhabit a buffered microenvironment (Carignan 1985) whose chemistry is largely controlled by physicochernicd reactions at the sediment-water interface. Consequently, this particular diatom record may be less subject to short-term seasonal fluctuations than most diatom records. Finally, mallomonadacean ckysophytes probably do not experience the kinds of Zag periods between microfossil production and representation in deepwater sediments that are experienced by benthic diatoms, developing in littoral habitats and subject to sedimentary transport processes (Sweets 1983) - although we recognize that this latter factor may be less important in a site as small as Cone Pond. For all these reasons, we suggest that chrysophyte assemblages are more likely to reflect temporally restricted conditions (such as snowmelt conditions) whereas sedimentary diatom assemblages may integrate lake water conditions over different seasons, as well as different habitats. Because changes in the chysophyte community parallel apparent changes in Cone Pond's fish population, and because fish and chrysophytes are known or at least suspected to be sensitive to metal loadings, changes in the concentration, complexation, or speciation of metals may be major factors in changes in both fish and chrysophyte communities. Metals, especially Al, have beenimplicatedas a causal factor in fish kills in acidified lakes (Muniz and Leivestad 1980). Because metal csncentratio~msand pH are often inversely related, it is difficult to assess the effects of each of these on chrysophyte communities. However, a regional survey of Adirondack lakes demonstrated strong relationships between metals and chrysophytes (Smol et al. 1984a). Four factors were particulaly marked: (1) M. hiaadoreii was most abundant in lakes with the highest Al concentrations whereas M . crassisquama exhibited the opposite pattern; (2) M. hiatdonii was a common taxon in the g o u p of lakes that shared several characteristics including low pH and high total Al concentrations; ( 3 ) M.hindonii was rare in acidic bog lakes; and (4) statistically significant conelations were determined for total A1 concentrations with the first reciprocal averaging axis determined for chrysophyte assemblages. Finally, Dixit (1986) presented some preliminary paleoli~namaological data suggesting that several chrysophyte species are sensitive to metal pollution. Anthropogenic acidification appears to be associated with changes in lake water metal chemistry because (1) AH, Mn, Be, Can. 9. Fish. Aguat. Sci., Mol. 44,6987


Cu, Hg, and Ni all undergo changes in speciation as pH decreases from 4.0 to 4.0 (Mudroch et al. 1984; National Research Council 1985), (2) increasing lake acidification mobilizes sedimentary metals (Schindler and Turner 1982; Norton 1983; KAl et al. 19841, and (3) both natural and anthropgenic changes in soil acidity increase lake loadings of acid-labile AI (National Research Council 1985; Ford and White 1986). Furthermore, anthropogenic acidification may lead to increased transparency in organically stained lake waters (Almer et al. 1978; Davis et al. 1985), presumably decreasing metal chelation capacity and thereby increasing metal toxicity (Patrick et al. 1981).

Conclusions The chrgrsophyte and diatom records at Cone Pond appear to disagree with respect to the extent and severity of recent anthropogenic acidification. This is an unusual situation, given the large number of studies in which diatoms and chrysophytes have provided corroborative information on trajectories of lake responses to acidification. However, many physical, chemical, and biological variables influence the size and composition of freshwater communities, and although pH has often been correlated with changes in fossil algal assemblages, it is well recognized that lakes with similar pH's may have very different limnological characteristics. In the case of the Cone Pond record, we looked for an explanation in which recent changes in lake water chemistry are superimposed on a presettlement background of strongly acid conditions. Transient changes in lake water chemistry associated with spring snowmelt provide such an explanation. Such changes would be characteristic of most sensitive first-order lakes in m a s receiving acidic precipitation and would be most likely to be tracked by vernal-blooming euplarnktonic Mallomonadaceae. The diatom flora, on the other hand, is composed of an m a y of ecologically diverse taxa that differ in habitat and phenology and may therefore be more sluggish in its overall response to such seasonally specific events. This hypothesis would also explain why, in lakes that have had their alkalinity exhausted by anthropogenic acidification, changes in chrysophyte assemblages are asynchronous with changes in the more spatially and temporally heterogenous diatom assemblages. Our data illustrate the importance of including both microfossil groups in lake reconstructions.

Acknowledgments This study was funded by thc Natural Sciences and Engineering Research Council of Canada by grants to JPS. We gratefully acbowledge the many useful comments we received from many scientists involved with the Pdeoecological Investigation of Recent Lake Acidification (PIRLA) project.

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