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12-2014

Radiocarbon Dating Suitability of Aquatic Plant Macrofossils James Marty Utah State University

Amy Myrbo Utah State University

Follow this and additional works at: http://digitalcommons.usu.edu/wats_facpub Part of the Life Sciences Commons Recommended Citation Marty, James and Myrbo, Amy, "Radiocarbon Dating Suitability of Aquatic Plant Macrofossils" (2014). Watershed Sciences Faculty Publications. Paper 854. http://digitalcommons.usu.edu/wats_facpub/854

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Journal of Paleolimnology Radiocarbon dating suitability of aquatic plant macrofossils --Manuscript Draft-Manuscript Number:

JOPL-D-13-00101R1

Full Title:

Radiocarbon dating suitability of aquatic plant macrofossils

Article Type:

Notes

Keywords:

Radiocarbon dating; Lake sediments; Plant macrofossils; Emergent aquatic plants; Submerged aquatic plants; Dissolved inorganic carbon (DIC)

Corresponding Author:

James Marty Utah State University Logan, UNITED STATES

Corresponding Author Secondary Information: Corresponding Author's Institution:

Utah State University

Corresponding Author's Secondary Institution: First Author:

James Marty

First Author Secondary Information: Order of Authors:

James Marty Amy Myrbo, PhD

Order of Authors Secondary Information: Abstract:

Paleolimnological and plant physiological literature were reviewed to determine which types of aquatic plant macrofossils are suitable for radiocarbon dating, with a particular focus on the uptake of reservoir-aged dissolved inorganic carbon (DIC) by emergent plants. Submerged aquatic plants utilize large amounts of DIC and are clearly not suitable for radiocarbon dating. Under certain environmental conditions, some emergent aquatic plants can metabolize DIC in quantities large enough to introduce old-carbon error to radiocarbon dates acquired from their remains (plant macrofossils). Over 300 plant macrofossil images are included in the online resource TMI (Tool for Microscopic Identification; http://tmi.laccore.umn.edu) along with guidance on identification and suitability for radiocarbon dating.

Response to Reviewers:

General responses to Reviewer #1: We feel that some of reviewer’s comments did not take into account that this is a review article, whose purpose is to summarize and synthesize the literature. In some cases we disagree with the reviewer; in these cases we have detailed our reasons and cited appropriate literature to support our preference not to make the requested changes. Reviewer #1: Journal of Paleolimnology JOPL-D-13-00101 Radiocarbon dating suitability of aquatic plant macrofossils James Marty and Amy Myrbo Objectives of the study This paper reviews the paleolimnological and plant physiological literature dealing with the suitability of aquatic plant macrofossils for radiocarbon dating. The limiting factor is the necessity to apply a not exactly known reservoir-correction. About 300 plants are screened compiled in the online archive TMI (tool for microscopic identification). Review of single sections The Section "Alternate sources of carbon" should begin with a compressed description of the system "lake water" with respect to the 14C dating. The presentation contains most elements but not didactically well ordered. Submerged and emergent plants may

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uptake atmospheric CO2 as well as CO2 dissolved in the lake water. Only the 14C value of atmospheric CO2 with the reference 14C value of 100 pMC (percent modern carbon) yields accurate 14C dates which can be calibrated. The dissolved CO2 in lake water is part of the dissolved inorganic carbon (DIC ≡ CO2* + HCO3- + CO32-; all DIC components have the same 14C value (neglecting the small differences due to isotope fractionation; Mook 1970) which is usually depleted in 14C compared of atmospheric CO2. The reservoir effect describes the involved processes. The main cause is the influx of groundwater or/and river water with depleted 14C of DIC into the lake. Additional causes are the decomposition of aged organic lake sediments by bacteria and the dissolution of bed rocks of lakes by dissolved excess CO2 or volcanic CO2. Therefore, all submerged organic material is affected by the reservoir effect and not suitable for precise 14C dating (The supersaturation of CO2 in lakes mentioned in the MS does not take into account that the dissolved CO2 and its origin changes with the season. Supersaturation occurs only after well-mixing of the lake in winter and the decomposition of organic matter. It disappears rapidly at least in the epilimnion when plants start to assimilate and organic matter is formed. At the end of the spring under¬saturation CO2 commences in the upper lake water and diffusion of atmospheric CO2 partly compensates the rising deficit. The 14C value in DIC is changed by these processes (e.g. Geyh et al. 1970) which explains its relationship with the ratio of lake surface and lake depth (Hakkanson 1979; Olsson 2009; Pazdur et al. 1980). Response: this important early section has been revised in response to the reviewer’s comments. Sentences have clearer didactic flow and connections to one another, and include each of the aspects that the reviewer wants included. The significance of supersaturation has been clarified within the context of atmospheric equilibrium. In the Section "Submerged aquatic vegetation use of DIC" the utilization, use or uptake of HCO3- by plants is frequently stated. Plants developed the process of photosynthesis during their genesis transforming CO2 into organic compounds. It is questioned that an additional metabolism developed for HCO3-. In any aqueous environment always CO2 is present. It is required to keep the HCO3- in solution. When the CO2-HCO3- equilibrium becomes disturbed (e.g. by consumption of CO2 by assimilation) HCO3- decomposes to CO32- and CO2 (Eq. 3). Therefore submerged plants sometimes bear crusts of carbonate. (1) CO2 + H2O ⇔ H+ + HCO3(2) HCO3- ⇔ CO32- + H+ (3) 2 HCO3- + Ca2+ ⇔ CaCO3 + CO2 + H2O This interrelation between CO2 and HCO3- is not taken into account in the Section "Emergent aquatic vegetation use of DIC". Therefore the sentence in P6L26 may be corrected to … emergent plants take up and assimilate CO2 as part of DIC from aquatic sources. Response: The use of HCO3- by submerged plants is well documented (Raven 1970, Walker et al. 1980, Allen and Spence 1981, Maberly and Spence 1983, Maberly and Madsen 2002). Perhaps the confusion is due to the word “use”. While ultimately the plant converts HCO3- to CO2 for photosynthesis, the starting point is HCO3- and the plant is responsible for conversion to CO2. The statement of “use” and “uptake” refers to the mechanism of HCO3- as a carbon source. The precedent for this language is established in the physiological literature (Raven 1970, Walker et al. 1980, Allen and Spence 1981, Maberly and Spence 1983, Maberly and Madsen 2002). Raven, J. A. (1970). Exogenous inorganic carbon sources in plant photosynthesis. Biological Reviews, 45, 167-221. Walker, N. A., Smith, F. A. & Cathers, I. R. (1980). Bicarbonate assimilation by freshwater charophytes and higher plants: I membrane transport of bicarbonate ions is not proven. Journal of Membrane Biology, 57, 51-58. Allen ED, Spence DHN (1981) The differential ability of aquatic plants to utilize the inorganic carbon supply in freshwaters. New Phytologist 87, 269–283. Maberly SC, Spence DHN (1983) Photosynthetic inorganic carbon use by freshwater plants. Journal of Ecology 71, 705–724. Maberly SC, Madsen TV (2002) Freshwater angiosperm carbon concentrating mechanisms: processes and patterns. Functional Plant Biology 29, 393-405.

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The scientific spelling has to be improved. Especially the scientific terms related to the hydrochemistry are misleading or ambiguous. Detailed comments and corrections Text P4 L12 include branches, wood pieces and charcoal Response: Wood pieces and branches are generally not considered good dating targets, because of the long lifetime of trees and the potential for them to persist on the landscape for long periods after death but before being transported into the lake. In our opinion it is not appropriate to include them in this list. Charcoal, if properly selected, is an excellent dating material, but macroscopic charcoal has the same problems as listed above for tree material. Only microscopic charcoal, derived from the burning of annual growth such as grasses and leaves, should be dated. Therefore we argue that none of the reviewer’s three suggested materials are “generally accepted as the best materials . . .” Microcharcoal, though desirable, is not a macroremain and thus is not included in this list of macrofossils. We respectfully decline to make this change. P4 L15 & L48 Replace Bjorck by Björck or at least Bjoerck Response: Done. P4 L17 replace dating by … precise (or accurate) 14C dating because many of these plants have depleted 14C values with respect to atmospheric CO2. Response: Done. P4 L19 replace history by suitability Response: This would change the meaning of the sentence. Suitability is already addressed at the end of the sentence (“. . . providing reliable and accurate dates”); “history” here refers to the literature. Reworded the sentence to make this clear. P4 L20 … fix DIC in the lake water with a depleted 14C value referring to atmospheric CO2, … Response: This is redundant, as this issue has been mentioned in the previous sentence. Also, the literature is essentially silent on CO2 vs DIC uptake with reference to 14C, so it is not appropriate to suggest that our paper includes such a summary. It only draws inferences about 14C implications based upon the information on DIC vs CO2 uptake. We respectfully decline to make this change. P4 L22 replace the incorrect sentence behind c) … by c) to quantify the depletion of 14C (reservoir effect) with respect to the 14C age. Response: Done. P4 L26 replace by Different sources of carbon in aquatic plants Response: Changed to “Alternate sources of carbon to aquatic plants.” “Alternate” is a better word choice in English. P4 L26-51 Rephrase this chapter. It should be didactically improved and has also to explain the reservoir effect. The hydrochemical processes have to be discussed also with respect to 14C. See the dedicated remarks in Review of single sections (above). Response: See responses above to the referenced section. P4 L31 plants take up most probably only dissolved CO2 which is part of DIC. It is produced from HCO3- as soon as its concentration drops below that of the dissolution equilibrium (Eq. 3). Response: this may be the case, but the literature in this review discusses HCO3 as a probable other source. We have reworded the sentence to include both CO2 and HCO3. As a simplification we frequently use “DIC” to include both CO2 and HCO3-. P4 L45 All submerged organisms (organic matter) are affected by the same reservoir effect (neglecting the minor effect of isotope fractionation between 12C, 13C and 14C). Hence, when organisms use submerged carbon sources their 14C value does not further change. Response: Clarified this sentence.

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P4 L49 Climatic, seasonal and other … Reponse: Changed. P5 L21 … that are usually spuriously too old Response: Changed. P5 L23 … rejected, as dating material yielding accurate 14C dates. Response: We suggest that this is an unneccesary and redundant addition of a few words. (It is not mentioned in this paper that the reservoir-effect ranges from zero to usually maximum 1000 years and can be considered as constant for sediments deposited in lakes with temporal constant depth. Response: We do not wish in this paper to review the reservoir effect itself; that subject has been addressed in numerous papers, a few of which we cite here. In these cases submerged material can be successfully dated and calibrated by single 14C dates of terrestrial macro rests. Moreover, it is not mentioned that terrestrial macrofossils sometimes yield stratigraphically inconsistent 14C ages if they were dislocated. Hence, it seems to be not correct that recommend universally rejecting submerged material from 14C dating. Response: We are reporting statements in the literature, not our own findings; we have added references to support our statement that submerged vegetation is “almost universally rejected” in the literature. Note that in the subsequent section where we discuss submerged macrofossils in more detail, we do (as suggested) state that in some cases (for certain types of lakes), submerged plant remains can be used. As for the issues with reworked or otherwise stratigraphically incorrect terrestrial macrofossils, we feel that this is outside the scope of this review paper, and that the subject has been addressed in many publications already.

P5 L36 Here should be added that even such small errors do exclude the possibility to calibrate the corresponding 14C dates. Response: Unclear - does the reviewer mean “do not exclude”? The issue of the calibration of 14C ages is quite a different (and well-described) issue and is not the topic of this paper. P5 L38 The following sentence suggests that the errors by the reservoir-effect were not thoroughly investigated. The 14C society knows that the reservoir effect of is extremely variable and differs from lake to lake. Therefore a uniform correction model cannot be expected. Response: Added clarifying sentence and removed material that was objectionable to the reviewer. P5 L48 … vegetation are plants … or better (but still not correct )… is a plant community … → Wikipedia definition Response: Deleted. P5 L49 It is doubted that any of the mentioned papers states that submerged vegetation takes up HCO3- dissolved in the lake water Response: See response to query about HCO3- mechanism above. (aquatic HCO3- seems to be funny expression). Reponse: changed to “aqueous HCO3-” here and earlier in the ms where this term appears There are various metabolism processes of CO2 rather than any of HCO3-. Because HCO3- is kept in solution only under a quantitatively well-known concentration of CO2, any deficit of the latter results in a decomposition of HCO3- into H2O and CO3-. Hence, it is more energy efficient to uptake dissolved CO2 rather than HCO3-. Check seriously this assumption. Response: See response to query about HCO3- mechanism above. DIC in lakes is seldom derived from "bedrock". It is usually imported with groundwater Powered by Editorial Manager® and ProduXion Manager® from Aries Systems Corporation

or river water which gathers the carbonate from the top sediments in the catchment area during the seepage of rain water. Response: the use of “bedrock” is intended to indicate the ultimate source of old C i.e., frequently radiocarbon-dead carbonate bedrock (marine limestone, for instance). While this material may be weathered physically or chemically (e.g., by glacial activity that pulverizes it) into “top sediments in the catchment area,” the ultimate source, and the cause of the old C problem, is the dead C in (e.g.) old limestone. We prefer to leave in the term “bedrock” because there are numerous lakes formed in bedrock (e.g., in karst regions) or receiving runoff from carbonate bedrock (e.g., in montane regions), but have added “or surficial material,” which we agree was erroneously missing from the earlier version. P5 L54 Any CO2 dissolved in pore or lake water is affected by the reservoir effect! Reject subordinate clause. Response: deleted. P5 L58 Within the belt of moderate climate any lake is well-mixed during winter time and develops stratigraphical differentiation (hypolymnion, epilimnion) during the warm season. If you disagree, explain the term well-mixed lakes. Response: Paleolimnological studies often seek lakes that are not well-mixed, i.e., those that are density-stratified over longer terms than seasonally, because such lakes may persistently lack oxygen in their hypolimnia and thus preserve sediment laminations by excluding burrowing fauna. For this reason we note the exception of well-mixed lakes - because they are probably rare as the focus of paleolimnological studies. P6 L4 Submerged organic material is generally affected by the reservoir effect (Olsson 2009) and it is never rare. Reponse: We believe that the reviewer is actually in agreement with our statement and has perhaps misinterpreted it. P6 L25 Most probably it is more correct or at least non-questionable to write … assimilate dissolved CO2 rather than … assimilate DIC. Reponse: we respectfully disagree, given the references listed here that say that plants take up HCO3-. We believe that using “DIC” here is better because it includes both CO2 and HCO3- and does not make a judgment on previous literature that does state that HCO3- is used. P6 L44 Most probably it is more correct or at least non-questionable to write … enhance uptake of dissolved CO2 rather than … enhance DIC uptake. Response: Same as previous - we find DIC to be a more inclusive term. P6 L51 Correct is: By definition concentration = mass/volume has no plural. Response: Corrected. P7 L14 Taking into account that you like to investigate the effect of the reservoir effect to the 14C ages, the use of DIC in this clause seems to be justified in opposite to all former mentioned descriptions of this topics. Response: OK, thank you. P7 L55 This estimate is trivial and can be deleted. The user does never know the actual 14C depletion in a sample without a dedicated study of the lake system to be dated. It may be more helpful to give ranges of the reservoir effect and their effect to the 14C age. Response: Added citation to Table 1, which includes the references to these estimates from the literature. P8 L16 This recommendation is questioned and might be deleted. You have 300 different plants which may have different reservoir-effects varying under changing environmental conditions. Such a recommendation would only be acceptable for most frequently found and dated macrofossils if such material exists. Even in this case extraordinary extended research is required to consider all imaginable lake environments and seasons of plant growth. Response: We respectfully disagree that more research is not warranted in this field. Powered by Editorial Manager® and ProduXion Manager® from Aries Systems Corporation

Patterns might emerge between plants of different habitats, and it might be found that DIC uptake is trivial in some types of plants that are held in suspicion. We would prefer to keep the recommendation. P8 L22 Your MS is no guide for a deliberate consideration of the carbon source and the potential for reservoir-corrected error. It may be doubted that any exists. Otherwise a reservoir-correction would be possible and reliable. Reject this sentence. Response: We believe that the reviewer misconstrued this sentence. We have revised it to clarify that we are simply talking about consideration of specific samples, which can be identified and evaluated using TMI and this ms., not about trying to correct one’s reservoir effect. P8 L48 Are the author of the early version Jimmy Marty identical with the author of this review paper James Marty? Response: Yes. References being not correctly cited General the references in the text have to be ordered according to the year of publication or alphabetically rather than chaotic. Response: All instances reordered according to chronology. Missing references in the text which are found in the reference list: P5L55 Maberly 1985 . P6L43 Mommer et al. 2007 rather than Mommer et al. 2005 ? P12L21 Kilian et al. 1995 P13L39 Mook 1980 P16L43 Wohlfarth et al. 1998 Response: Changed Cited references in the text missing in the reference list P6L19 Jackson 1985 P7L45 Kilian et al. 2000 Response: Changed Figures Fig. 1: May be deleted as the information is trivial and not usable in practice due to even missing estimates of the 14C depletion in a sample to be dated Response: We agree that this figure might be seen as trivial; however, its purpose is to illustrate the “ballpark” ranges of age error and how much certain reservoirs can change one’s estimated age, not “usable” in terms of assisting the reader in calculating the error in one’s ages. Slightly modified figure caption to reflect this purpose.

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Manuscript Click here to download Manuscript: Marty_Myrbo_JoPLsubmission_20140829_Wrefs.doc Click here to view linked References 1 2 3 4 Radiocarbon dating suitability of aquatic plant macrofossils 5 6 James Marty (corresponding author) 7 8 Ecology Center and Department of Watershed Sciences, Quinney College of Natural 9 Resources, Utah State University, Logan, UT, 84321 10 [email protected] 11 12 13 Amy Myrbo 14 LacCore, Department of Earth Sciences, University of Minnesota, Minneapolis, MN, 55455 15 [email protected] 16 17 18 Keywords: 19 Radiocarbon dating 20 21 Lake sediments 22 Plant macrofossils 23 Emergent aquatic plants 24 Submerged aquatic plants 25 26 Dissolved inorganic carbon (DIC) 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65

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Abstract Paleolimnological and plant physiological literature were reviewed to determine which types of aquatic plant macrofossils are suitable for radiocarbon dating, with a particular focus on the uptake of reservoir-aged dissolved inorganic carbon (DIC) by emergent plants. Submerged aquatic plants utilize large amounts of DIC and are clearly not suitable for radiocarbon dating. Under certain environmental conditions, some emergent aquatic plants can metabolize DIC in quantities large enough to introduce old-carbon error to radiocarbon dates acquired from their remains (plant macrofossils). Over 300 plant macrofossil images are included in the online resource TMI (Tool for Microscopic Identification; http://tmi.laccore.umn.edu) along with guidance on identification and suitability for radiocarbon dating.

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Introduction The macroscopic remains (macrofossils) of terrestrial plants, such as seeds, leaves, needles, and bracts, are generally accepted as the best materials for producing accurate radiocarbon dates in lacustrine sedimentary sequences (Deevey et al. 1954; Olsson 1983; Marcenko et al. 1989; Björck and Wohlfarth 2002; Birks 2002; Olsson 2009; Grimm et al. 2011). Macrofossils of aquatic plants are frequently present in lake sediment cores as well, but may not be suitable for precise or accurate radiocarbon dating because many of these plants have depleted 14C values with respect to atmospheric CO2, due to their use of dissolved inorganic carbon (DIC ≡ CO2* + HCO3- + CO32-) in addition to or in place of atmospheric CO2. This note reviews the existing literature with respect to a) the history of reliable and accurate dates derived from aquatic plants of different habits, b) the ability of submerged and emergent aquatic plants to fix DIC vs. atmospheric CO2, and c) the depletion of 14C (the “reservoir effect”) with respect to the 14C age of photosynthetically fixed carbon in plant materials. Alternate sources of carbon to aquatic plants Terrestrial plants fix almost exclusively atmospheric CO2 for photosynthetic use; however, plants of aquatic ecological habits are exposed to and can take up CO2 or HCO3- from DIC as well as atmospheric CO2. In physically well-mixed or low-alkalinity aquatic systems, dissolved CO2 may be in equilibrium with atmospheric CO2 with respect to partial pressure and isotopic composition, but in most lakes DIC incorporates C from other sources in addition to the atmosphere (Cole and Caraco 2001, Myrbo and Shapley 2006), and photosynthesis removes CO2 from the epilimnion rapidly during the growing season. Lakes are thus more commonly oversaturated or undersaturated than in equilibrium with respect to CO2 (Cole et al. 1994, Myrbo and Shapley 2006). Carbon derived from non-atmospheric sources is typically depleted in 14C relative to contemporaneous atmospheric CO2 (Godwin 1951; Broecker and Orr 1958), and is the source of the old carbon “reservoir effect” (Olsson 1980) that imparts an artificially old age to aquatic plant tissue. The reservoir effect is commonly associated with hardwater lakes having high concentrations of DIC derived from the dissolution of carbonate rocks, but other processes such as the oxidation of soil or other old organic matter (Cole et al. 2001), infrequent mixing (in lakes with high surface-area-to-depth ratios; Hakkanson 1979; Olsson 2009), and respiration of CO2 derived from organisms that fix DIC (MacDonald et al. 1987) are also sources of old C. This list does not include processes in arctic and volcanic regions, which may be old-CO2 enriched for numerous other reasons (Björck and Wohlfarth 2002). Climatic, seasonal, and other environmental changes can alter the rates of the above mentioned processes, and so the radiocarbon reservoir age of a given lake may not be constant over time (Geyh et al. 1999). Emergent plants

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Emergent plants are generally defined as plants rooted beneath the water but with mostly aerial vegetation (Cronk and Fennessy 2001). This broad definition fails to capture the breadth of plant growth forms adapted to life at the aquatic-terrestrial interface. For example, individual Juncus bulbosus L. may either grow submerged in shallow water or terrestrially along the shoreline for the entirety of a growing season (Hitchcock et al. 1969). Stratiotes aloides L. is a free floating (unrooted) aquatic plant with submerged and aerial leaves (Nielsen and Borum 2008). The phenology of Zizania palustris L. involves growth at submerged, floating leaf, and aerial leaf stages (Weir and Dale 1960). For the purposes of this note, emergent aquatic vegetation are defined as plants that may experience both atmospheric and aquatic environments under natural conditions. History of dating aquatic plant macrofossils It is well documented that macrofossils from submerged vegetation and aquatic mosses often return radiocarbon dates that are spuriously old (Deevey et al. 1954; Hakkanson 1979; Olsson 1983; Birks 2002). Terrestrial macrofossils are almost universally recommended, and submerged macrofossils rejected (Birks 2002 and references therein), as radiocarbon dating material; yet the gray area presented by emergent vegetation is largely unacknowledged in paleolimnological literature. Birks (2002) suggests avoiding wetland species such as Schoenoplectus due to large intercellular spaces with high concentrations of CO2. Macrofossils of emergent vegetation have a strong history of providing good dates (Deevey et al. 1954; Heikkinen et al. 1977; Hakansson 1982; Tornqvist et al. 1992; Lowe et al. 2004; Grimm 2011). Yet there are some cases of each vegetation type returning dates that are too old (Damon et al. 1964; Haynes et al. 1966; Tornqvist et al. 1992; Turney et al. 2000; Wasylikowa and Walanus 2004; Edwards et al. 2011). Certain emergent aquatic plant characteristics such as the growth pattern of Sphagnum mosses and isotopic fractionation through the C4 photosynthetic pathway can result in small errors in radiocarbon age, but do not explain larger errors (Chivas et al. 2001; Goslar et al. 2005). Olsson (1983) demonstrated that emergent and floating leaved vegetation have lower 14C activities than terrestrial vegetation, though not as low as submerged aquatics. Because emergent vegetation occupies a transitional zone where both atmospheric and aquatic sources of CO2 are available, the possibility that emergent aquatics are utilizing reservoir aged carbon therefore warrants further investigation. Submerged aquatic vegetation use of DIC Most submerged aquatic vegetation are able to take up aqueous HCO3- derived from carbonate bedrock or surficial material that results in radiocarbon dates many thousands of years too old (Spence and Maberly 1985; Sand-Jensen et al. 1992; Maberly and Madsen 2002). Aquatic mosses and some submerged vegetation do not utilize HCO3-; rather they fix dissolved CO2 from the water column and sediment pore water (Spence and Maberly 1985; Sand-Jensen et al. 1992; Maberly and Madsen 2002). The submerged plant Vallisneria americana Michx. can use both HCO3- and dissolved CO2 from the water column and dissolved CO2 in the sediment pore water (Winkel and Borum 2009). In very well mixed, soft water lakes, it may be possible to date both submerged vegetation and aquatic mosses (Hakansson 1979; Miller et al. 1999; Oswald et

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al. 2005). However, complete absence of a reservoir effect is rare, and dating macrofossils of submerged vegetation and aquatic mosses is generally inadvisable (Olsson 2009). Emergent aquatic vegetation use of DIC Plant colonization of land 600-400 million years ago is associated with the evolution of stomata and the ability to exchange gases with the atmosphere. By overcoming the barriers of low gas diffusion rates and limited availability of light and free CO2 in the aquatic environment, terrestrial plants are able to uptake CO2 and photosynthesize at higher rates than submerged aquatic plants (Salvucci and Bowes 1982; Raven et al. 1985; Maberly and Spence 1989; Nielsen 1993; Raven and Edwards 2001; Clarke et al. 2011). Because many emergent aquatic plants have leaf morphologies resembling terrestrial plants, there is a general assumption that most emergent plants acquire the majority of their photosynthetic CO2 from the atmosphere (Wetzel 1975; Maberly and Madsen 2002). However, the physiological literature suggests that, under particular environmental conditions, there are a variety of mechanisms through which emergent plants can take up and assimilate DIC from aquatic sources (Table 1). Water column uptake of DIC The high diffusive resistance of aqueous CO2 inhibits gas exchange between terrestrially adapted plant tissue (characteristic of many emergent plants) and the aquatic environment (Raven 1984; Sand-Jensen and Frost-Christensen 1999). Many submerged aquatic plants have thin, elongate leaves with a high specific leaf area that allows for higher gas diffusion rates in the water column (Maberly and Spence 1989; Sand-Jensen and Frost-Christensen 1999; Mommer and Visser 2005). In addition to aerial leaves, heterophyllous (multiple leaf morphologies) emergent species are able to produce leaves very similar to the leaves of submerged aquatic plants (Hostrup and Wiegleb 1991; Frost-Christensen and Sand-Jensen 1995; Madsen and Breinholt 1995; Bruni et al. 1996; Maberly and Madsen 1998; Robe and Griffiths 1998; Garbey et al. 2004; Mommer and Visser 2005). The submerged leaves of these species enhance DIC uptake through passive diffusion in the water column, increase productivity, and can match photosynthetic rates of fully submerged plants (Sand-Jensen et al. 1992; Madsen and Breinholt 1995; Maberly and Madsen 1998). One heterophyllous free floating emergent, Stratiotes aloides L., possesses submerged leaves that can fix DIC in the form of HCO3- (Prins and De Guia 1986; Nielsen and Borum 2008). Some homophyllous (one leaf morphology) emergent species can photosynthesize effectively while submerged through passive diffusion, but only at very high CO2 concentration (Sand-Jensen et al. 1992). Another adaptation of emergent plants to submerged conditions are gas film layers of aerial leaves. When leaves are completely submerged (simulating flooded conditions), gas film layers mediate exchange of CO2 in the water column and can enhance photosynthesis for Phalaris arundinacea L., Phragmites australis (Cav.) Trin. Ex Steudel, and other emergent grasses (Colmer and Pedersen 2008; Winkel et al. 2011). The effect of gas film layers on CO 2 exchange under more ambient conditions of partial submergence is unknown. Root zone uptake of DIC

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It is well established that plants of the isoetid growth form are adept at utilizing dissolved CO2 in the sediment in low pH conditions. Isoetids are amphibious emergents, some almost exclusively growing submerged (Isoetes lacustris L.) or emergent (Eriocaulon decangulare L.).The quantities of DIC fixed by isoetids from the sediment range from 25% (Juncus bulbosus L.) to 99% (Lobelia dortmanna L.) (Wium-Andersen 1971; Richardson et al. 1984; Wetzel et al. 1985). Isoetids are taxonomically diverse but morphologically and physiologically very similar, and are characterized by a high root:shoot ratio and lack of stomata (Keeley et al. 1984). Emergent plants of other growth forms can also take up dissolved CO2 in the sediment. Found in similar environments to isoetids, Sparganium angustifolium Rehman utilizes dissolved CO2 from sediment pore water in amounts that significantly affect productivity, though exact mechanism and quantity are unknown (Lucassen et al. 2009). The large intercellular gas spaces (aerenchyma) recognized by Birks (2002) as a concern for the radiocarbon dating of emergent macrofossils create an efficient gas transport system and create a circulation network that allows the uptake and transport of sedimentary dissolved CO2 (in addition to atmospheric sourced respiratory CO2) from the sediment to the vegetative parts of the plant (Dacey and Klug 1979; Dacey and Klug 1982; Longstreth 1989; Constable et al. 1992). Nuphar lutea (L.) Sm., P. australis, Typha latifolia L., Spartina alterniflora Loisel., Schoenoplectus tabernaemontani (C.C. Gmel.) Palla, and Cyperus papyrus L. all possess aerenchyma with high concentrations of gaseous CO2 (Dacey and Klug 1982; Longstreth 1989; Brix 1990; Constable et al. 1992; Hwang and Morris 1992; Singer et al. 1994). Total sedimentary dissolved CO2 fixed as a percentage of all fixed carbon ranges from less than 0.25% to 10% to unknown for these species (Table 1). For plants that utilize small amounts of sedimentary CO2, it is hypothesized that sedimentary CO2 may only be important for young seedlings submerged in shallow water (Brix 1990; Singer et al. 1994). Some woody plants have the ability uptake DIC via the roots. Up to 2% of all carbon fixed by young Salix viminalis L. is taken up through the roots in hydroponic solution (Vapaavuori and Pelkonen 1985; Vuorinen et al. 1989). Aquatic mycorrhizal fungi associated with the roots of Ericaceae in bogs can facilitate root uptake of CO2 (Harley and Smith 1983; Allen 1991). While the contribution of mycorrhizal CO2 is suggested to be insignificant to aboveground carbon, dates of Ericaceae rootlets have been dated 100-150 years too old (Kilian et al. 1995). Effect of old (reservoir) CO2 on radiocarbon dating When aquatic plants do metabolize a combination of atmospheric and aqueous C, the apparent age of the plant tissue at the time of death (i.e., when the “radiocarbon clock” begins) is a product of the reservoir age of the aqueous DIC and the fraction of the total C taken up by the plant that is derived from that aqueous DIC (Figure 1). Neither of these quantities is likely to be well known; however, the few published data (Table 1) serve as a general guide. Emergent aquatic plants have the ability to assimilate aqueous DIC in varying quantities and through a diversity of mechanisms. However, it must be acknowledged that substantial use of DIC typically occurs only under particular environmental conditions such as supersaturation of CO2 in the water column or sediment and flooding. Furthermore, distribution of assimilated DIC within emergent plants is poorly understood. This is especially important considering the

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most common emergent plant macrofossils in lake sediments are typically fruits or seeds. Few studies trace the destination of metabolized DIC, and no studies specify at what stage of the reproductive cycle the study plants were in. Transport of photosynthate from source to sink in terrestrial agricultural plants is relatively local, but the aquatic system is markedly different (Stoy 1965; Bartkov and Zvereva 1974; Larcher 2003). Experimental work using isotopic tracers in atmospheric CO2 and DIC would clarify the magnitude and timing of aqueous C uptake, and its distribution among plant tissue types. Understanding the environmental characteristics and ecophysiology of the emergent vegetation within a catchment is vital to the selection of appropriate plant macrofossils for radiocarbon dating. Deliberate consideration of macrofossil samples with respect to their carbon source and the potential for reservoir-introduced error should be undertaken before submission of emergent plant macrofossils for radiocarbon dating.

Identification of plant macrofossils The identification and ecological interpretation of subfossil plant remains in lake sediments requires expertise and physical reference materials. Nonspecialists, however, can take advantage of a large collection (>300) of high-resolution photographs tagged with information on taxonomy, identification, and suitability for radiocarbon dating, part of the free online resource TMI (Tool for Microscopic Identification, http://tmi.laccore.umn.edu; Myrbo et al., 2011). Specimens in the database include taxa mainly found in central North America and the Rocky Mountains of the United States, but represent cosmopolitan families and genera that can be found in many parts of the world.

Note: an early version of this review appears as the tutorial “‘Do not date’ list: radiocarbon dating of macroscopic plant remains” on TMI (http://tmi.laccore.umn.edu) Acknowledgments: The authors gratefully acknowledge Dick Baker, Iowa State University, for gracious access to his plant macrofossil reference collection and imaging system. TMI and this work have been supported by NSF-EAR-1226265 and a University of Minnesota Interdisciplinary Informatics Seed Grant.

References Allen, M.F. 1991. The ecology of mycorrhizae. Cambridge University Press, New York, 184 pp. Bartkov, B.I., and Zvereva, G. 1974. Raspredelenie assimiliatov v period plodonosheniya bobovykh rastenii. O printcipe dublirovaniya v fitosistemakh. Fiziol i Biokhimiya Kult. Rast. 6: 502-505.

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65

Birks, H.H. 2002. Plant macrofossils. In: Smol, J.P., Birks, H.J.B., Last, W.M. (Eds.), Tracking Environmental Change Using Lake Sediments, vol. 3: Terrestrial, Algal, and Siliceous Indicators. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 49-74. Björck, S., and Wohlfarth, B. 2002. 14C chronostratigraphic techniques in paleolimnology. In: Smol, J.P., Birks, H.J.B., Last, W.M. (Eds.), Tracking Environmental Change Using Lake Sediments, vol. 1: Basin Analysis, Coring, and Chronological Techniques. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 205-245. Brix, H. 1990. Uptake and photosynthetic utilization of sediment-derived carbon by Phragmites australis (Cav.) Trin. ex Steudel. Aquat. Bot. 38: 377-389. Broecker, W.S., and Orr, P.C. 1958. Radiocarbon chronology of Lake Lahontan and Lake Bonneville. Geol. Soc. Am. Bull. 69: 1009-1032. Bruni, N.C., Young, J.P., and Dengler, N.C. 1996. Leaf developmental plasticity of Ranunculus flabellaris in response to terrestrial and submerged environments. Can. J. Bot. 74: 823-837. Chivas, A.R., Garcia, A., van der Kaars, S., Couapel, Martine, J.J., Holt, S., Reeves, J.M., Wheeler, D.J., Switzer, A.D., Murray-Wallace, C.V., Banerjee, D., Price, D.M., Wang, S., X., Pearson, G., Edgar, T.N., Beaufort, L., de Deckker, P., Lawson, E., Cecil, C., B. 2001. Sealevel and environmental changes since the last interglacial in the Gulf of Carpentaria, Australia: an overview. Quatern. Int. 83-85: 19-46. Clarke, J.T., Warnock, R.C.M., Donoghue, P.C.J. 2011. Establishing a time-scale for plant evolution. New Phytol. 192: 266: 301. Cole, J.J., Caraco, N.F., Kling, G.W., Kratz, T.K. 1994. Carbon dioxide supersaturation in the surface waters of lakes. Science. 265: 1568-1570. Cole, J.J., and Caraco, N.F. 2001. Carbon in catchments: connecting terrestrial carbon losses with aquatic metabolism. Mar. Environ. Res. 52: 101-110. Colmer, T.D., and Pedersen, O. 2008. Underwater photosynthesis and respiration in leaves of submerged wetland plants: gas films improve CO2 and O2 exchange. New Phytol. 177: 918-926. Constable, J.V.H., Grace, J.B., and Longstreth, D.J. 1992. High carbon dioxide concentrations in aerynchyma of Typha latifolia. Am. J. Bot. 79: 415-418. Cronk,J.K., and Fennessy, M.S. 2001. Wetland plants: biology and ecology. Lewis Publishers, Boca Raton, Florida, pp. 7-12. Dacey, J.W.H., and Klug, M.J. 1979. Methane efflux from lake sediments through water lilies.

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65

Science. 203: 1253-1255. Dacey, J.W.H., and Klug, M.J. 1982. Tracer studies of gas circulation in Nuphar: 18O2 and 14CO2 transport. Plant Physiol. 56: 361-366. Damon, P.E., Haynes, C.V., and Long, A. 1964. Arizona radiocarbon dates V. Radiocarbon. 6: 91-107. Deevey, E.S., Gross, M.S., Hutchinson, G.E., and Kraybill, H.L. 1954. The natural C14 contents of materials from hard-water lakes. Geology. 40: 285-288. Edwards, K.J., Schofield, J.E., Kirby, J.R., and Cook, G.T. 2011. Problematic but promising ponds? Palaeoenvironmental evidence from the Norse Eastern Settlement of Greenland. J. Quaternary Sci. 26: 854-865. Frost-Christensen, H., and Sand-Jensen, K. 1995. Comparative kinetics of photosynthesis in floating and submerged Potamogeton leaves. Aquat. Bot. 51: 121-134. Garbey, C., Thiebaut, G., and Muller, S. 2004. Morphological plasticity of a spreading aquatic macrophyte, Ranunculus peltatus, in response to environmental variables. Plant Ecol. 173: 125137. Geyh, M.A., Grosjean, M., Núñez, L. Schotterer, U. 1999. Radiocarbon reservoir effect and the timeng of the late-glacial/early Holocene phase in the Atacama Desert (northern Chile). Quat. Res. 52: 143-153. Godwin, H. 1951. Comments on radiocarbon dating for samples from the British Isles. Am. J. Sci. 249: 301-307. Goslar, T., van der Knaap, W.O., Hicks, S., Andric, M., Czernik, J., Goslar, E., Rasanen, S., Hyotyla, H. 2005. Radiocarbon. 47: 115-134. Grimm, E.C. 2011. High-resolution age model based on AMS radiocarbon ages for Kettle Lake, North Dakota, USA. Radiocarbon. 53: 39-53. Hakansson S. 1979. Radiocarbon activity in submerged plants from various south Swedish lakes. In: Berger, R., and Suess, H.E. (Eds.), Radiocarbon Dating: Proceedings of the Ninth International Conference. University of California Press, pp. 433-443. Hakansson S. 1982. University of Lund radiocarbon dates XV. Radiocarbon. 24: 194-213. Harley, J.L., and Smith, S.E. 1983. Mycorrhizal symbiosis. Academic Press, New York, 483 pp. Haynes, C.V., Damon, P.E., and D.C. Grey. 1966. Arizona radiocarbon dates VI. Radiocarbon.

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65

8:1-21. Heikkinen, A., and Aikaa, O. 1977. Geological survey of Finland radiocarbon measurements VII. Radiocarbon. 19: 263-279. Hitchcock, C.L., Cronquist, A., Ownbey, M., and Thompson, J.W. 1969. Vascular plants of the Pacific Northwest. University of Washington Press, Seattle. Hostrup, O., and Wiegleb, G. 1991. Anatomy of leaves of submerged and emergent forms of Littorella uniflora (L.) Ascherson. Aq. Bot. 39: 195-209. Hwang, Y., and Morris, J.T. 1992. Fixation of inorganic carbon from different sources and its translocation in Spartina alterniflora Loisel. Aquat. Bot. 43: 137-147. Higuchi, T., Yoda, K., and Tensho, K. 1984. Further evidence for gaseous CO2 transport in relation to root uptake of CO2 in rice plant: Soil Sci. Plant Nutr. 30: 125-136. Keeley, J.E., Osmond, C.B., and Raven, J.A. 1984. Stylites, a vascular land plant without stomata absorbs CO2 via its roots. Nature. 310: 694-695. Kilian, M.R., Van Der Plicht, J., and Van Geel, B. 1995. Dating raised bogs: new aspects of 14C wiggle matching, a reservoir effect, and climatic change. Quat. Sci. Rev. 14: 959-966. Larcher, W. 2003. Physiological plant ecology. Springer, Berlin, Germany, pp. 149-150. Longstreth, D.J. 1989. Photosynthesis and photorespiration in freshwater emergent and floating plants. Aquat. Bot. 34: 287-299. Lowe, J.J., Walker, M.J.C., Scott, E.M., Harkness, D.D., Bryant, C.L., and Davies, S.M. 2004. A coherent high-precision radiocarbon chronology for the Late-glacial sequence at Sluggan Bog, Co. Antrim, Northern Ireland. J. Quaternary Sci. 19: 147-158. Lucassen, E.C.H.E.T., Spierenburg, P., Fraaije, R.G.A., Smolders, A.J.P., and Roelofs, J.G.M. 2009. Alkalinity generation and sediment CO2 uptake influence establishment of Sparganium angustifolium in softwater lakes. Freshwater Biol. 54: 2300-2314. Maberly, S.C., Spence, D.H.N. 1989. Photosynthesis and photorespiration in freshwater organisms: amphibious plants. Aquat. Bot. 34: 267-286. Maberly, S.C., and Madsen, T.V. 1998. Affinity for CO2 in relation to the ability of freshwater macrophytes to use HCO3-. Func. Ecol. 12: 99-106. Maberly, S.C., and Madsen, T.V. 2002. Freshwater angiosperm carbon concentrating mechanisms: processes and patterns. Funct. Plant Biol. 29: 393-405.

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65

Madsen, T.V., and Breinolt, M. 1995. Effects of air contact on growth, inorganic carbon sources, and nitrogen uptake by an amphibious freshwater macrophyte. Plant Physiol. 107: 149-154. MacDonald, G.M., Beukens, R.P., Kieser, W.E., and Vitt, D.H. 1987. Comparative radiocarbon dating of terrestrial plant macrofossils and aquatic moss from the “ice-free corridor” of western Canada. Geology. 15: 837-840. Marcenko, E., Srdoc, D., Golubic, S., Pezdic, J., and Head, M.J. 1989. Carbon uptake in aquatic plants deduced from their natural 13C and 14C content. Radiocarbon. 31: 785-794. Miller, G.H., Mode, W.N., Wolfe, A.P., Sauer, P.E., Bennike, O., Forman, S.L., Short, S.K., and Stafford, T.K. 1999. Stratified interglacial lacustrine sediments from Baffin Island, Arctic Canada: chronology and paleoenvironmental implications. Quaternary Sci. Rev. 18: 789-810. Mommer, L., and Visser, E.J.W. 2005. Underwater photosynthesis in flooded terrestrial plants: a matter of leaf plasticity. Ann. Bot. 96: 581-589. Myrbo, A., Morrison, A., and McEwan, R. (2011). Tool for Microscopic Identification (TMI). http://tmi.laccore.umn.edu. Accessed on 08 November 2013 Myrbo, A. and Shapley, M.D. 2006. Seasonal water-column dynamics of dissolved inorganic carbon stable isotopic compositions (δ13CDIC) in small hardwater lakes in Minnesota and Montana. Geochimica et Cosmochimica Acta 70:2699-2714. Nielsen, S.L. 1993. A comparison of aerial and submerged photosynthesis in some Danish amphibious plants. Aquat. Bot. 45: 27-40. Nielsen, L.T., and Borum, J. 2008. Why the free floating macrophyte Stratiotes aloides mainly grows in highly CO2-supersaturated waters. Aquat. Bot. 89: 379-384. Olsson, I.U. 1980. Radiocarbon dating of material from different reservoirs. In: Suess, H.E., and Berger, R. (Eds.), Radiocarbon Dating. UCLA Press, San Diego, pp. 613-618. Olsson, I.U. 1983. Dating non-terrestrial materials. In: Mook, W.G., and Waterbolk, H.T. (Eds.), Proceedings of the International Symposium 14C and Archaeology. PACT v. 8, pp. 277-294. Olsson, I.U. 2009. Radiocarbon dating history: early days, questions, and problems met: Radiocarbon. 51: 1-43. Oswald, W.W., Anderson, P.M., Brown, T.A., Brubaker, L.B., Hu, F.S., Lozhkin, A.V., Tinner, W., and Kaltenrieder, P. 2005. Effects of sample mass and macrofossil type on radiocarbon dating of arctic and boreal lake sediments. Holocene. 15: 758-767.

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65

Prins, H.B.A., and De Guia, M.B. 1986. Carbon source of the water soldier, Stratiotes aloides L. Aquat. Bot. 26: 225-234. Raven, J.A. 1984. Energetics and transport in aquatic plants. Alan R. Liss, New York. Raven, J.A., Osbourne, B.A., Johnston, A.M. 1985. Uptake of CO2 by aquatic vegetation. Plant Cell Environ. 8: 417-425. Raven, J.A., Handley, L.L., MacFarlane, J.J., McInroy, S., McKenzie, L., Richards, J.H., and Samuelsson, G. 1988. The role of CO2 uptake by roots and CAM in acquisition of inorganic C by plants of the isoetid life-form: a review, with new data on Eriocaulon decangulare L. New Phytol. 108: 125-148. Raven, J.A., and Edwards, D. 2001. Roots: evolutionary origins and biogeochemical significance. J. Exp. Bot. 52: 381-401. Richardson, K., Griffiths, H., Reed, M.L., Raven, J.A., and Griffiths, N.M. 1984. Inorganic carbon assimilation in the isoetids, Isoetes lacustris L. and Lobelia dortmanna L. Oecologia. 61: 115121. Robe, W.E., and Griffiths, H. 1998. Adaptations for amphibious life: changes in leaf morphology, growth rate, carbon and nitrogen investment, and reproduction during adjustment to emersion by the freshwater macrophyte Littorella uniflora. New Phytol. 140: 9-23. Salvucci, M.E., and Bowes, G. 1982. Photosynthetic and photorespiratory responses of aerial and submerged leaves of Myriophyllum brasiliense. Aquat. Bot. 13: 147-164. Sand-Jensen, K., Pederson, M.F., and Nielsen, S.L. 1992. Photosynthetic use of inorganic carbon among primary and secondary water plants in streams. Freshwater Biol. 27: 283-293. Sand-Jensen, K., and Frost-Christensen, H. 1999. Plant growth and photosynthesis in the transition zone between land and stream. Aq. Bot. 63: 23-35. Singer, A., Eshel, A., Agami, M., and Beer, S. 1994. The contribution of aerenchymal CO 2 to the photosynthesis of emergent and submerged culms of Scirpus lacustris and Cyperus papyrus. Aquat. Bot. 49: 107-116. Smits, A.J.M., De Lyon, M.J.H., Van Der Velde, G., Steentjes, P.L.M., Roelofs, J.G.M. 1988. Distribution of three nymphaeid macrophytes (Nymphaea alba L., Nuphar lutea (L.) Sm., and Nymphoides peltata (Gmel.) O. Kuntze) in relation to alkalinity and uptake of inorganic carbon. Aquat. Bot. 32: 45-62. Spence, D.H.N., and Maberly, S.C. 1985. Occurrence and ecological importance of HCO3- use

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65

among aquatic higher plants. In: Lucas, W.J., and Berry, J.A. (Eds.), Inorganic carbon uptake by aquatic photosynthetic organisms, Proceedings of an International Workshop on Bicarbonate Use in Photosynthesis, pp. 125-143. Stoy, V. 1965. Photosynthesis, respiration and carbohydrate accumulation in spring wheat in relation to yield. Physiol. Plant. 4: 1-125. Turney, C.S.M., Coope, G.R., Harkness, D.D., Lowe, J.J., and Walker, M.J.C. 2000. Implications for the dating of Wisconsian (Weichselian) late-glacial events of systematic radiocarbon age differences between terrestrial plant macrofossils from a site in SW Ireland: Quaternary Res. 53: 114-121. Vapaavuori, E.M., and Pelkonen, P. 1985. HCO3- uptake through the roots and its effect on the productivity of willow cuttings. Plant Cell Environ. 8: 531-534. Vuorinen A.H., Vapaavuori, E.M., and Lapinjoki, S. 1989. Time-course of uptake of dissolved inorganic carbon through willow roots in light and darkness. Physiol. Plantarum. 77: 33-38. Wasylikowa, K., and Walanus, A. 2004. Timing of aquatic and marsh-plant successions in different parts of Lake Zeribar, Iran, during the Late Glacial and Holocene. Acta Palaeobot. 44: 129-140. Weir, C.E., and Dale, H.M. 1960. A developmental study of wild rice, Zizania aquatica L. Can. J. Bot. 38: 719-741. Wetzel, R.G. 1975. Limnology. Thomson Learning, Michigan, 858 pp. Wetzel, R.G., Brammer, E.S., Lindstrom, K., and Forsberg, C. 1985. Photosynthesis of submersed macrophytes in acidified lakes II. Carbon limitation and utilization of benthic CO2 sources. Aquat. Bot. 22: 107-120. Winkel, A., and Borum, J. 2009. Use of sediment CO2 by submersed rooted plants. Ann. Bot. 103: 1015-1023. Winkel, A., Colmer, T.D., and Pedersen, O. 2011. Leaf gas films of Spartina anglica enhance rhizome and root oxygen during tidal submergence. Plant Cell Environ. 34: 2083-2092. Wium-Andersen, S. 1971. Photosynthetic uptake of free CO2 by the roots of Lobelia dortmanna. Plant Physiol. 25: 245-248.

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Figure 1. Plot simplistically illustrating how apparent age of plant tissue at death is affected by fraction of C taken up by a plant that is aqueous (dissolved inorganic carbon, DIC) and the reservoir age of the DIC. The three lines represent three different DIC reservoir ages. Table 1. Summary of emergent aquatic plants known to utilize some form of DIC. Taxa listed have not necessarily been examined for each carbon source; data shown are the only available. Key to “notes” column: 1. Species listed maintained productive photosynthetic rates while submersed; only applicable to high CO2 conditions; 2. Maintained productive photosynthetic rates while submersed; 3. DIC may be used by young seedlings/shoots; 4. 40% of DIC fixed was assimilated in the roots; 5. DIC was transported to shoots; 6. DIC was assimilated into young leaves and base of shoot; 7. Internal CO2 was not differentiated with respiratory CO2 but thought to be sediment derived; internal CO2 was a significant contributor to productivity.

table Click here to download Table: Marty_Myrbo_table1.pdf

Family

Species

Classification

Alismataceae

Sagittaria sagittifolia  L.

Submerged/Emergent

Atmospheric  Dissolved CO2  Dissolved CO2  (sediment) (water column) HCO3‐ Mechanism % DIC fixed  CO2 leaf and shoot passive diffusion; leaf  heterophylly x x unknown

Apiaceae

Berula erecta  (Hudson) Coville

Emergent

x

x

Apiaceae

Oenanthe aquatica  (L.) Poir.

Submerged/Emergent

x

Reference

Notes

Sand‐Jensen et al. 1992

1

Sand‐Jensen et al. 1992

1

x

leaf and shoot passive diffusion unknown leaf and shoot passive diffusion; leaf  heterophylly unknown

Mommer and Visser 2005

2 1

Boraginaceae

Myosotis laxa Lehm.

Emergent

x

x

leaf and shoot passive diffusion

unknown

Sand‐Jensen et al. 1992

Boraginaceae

Myosotis palustris  L.

Emergent

x

x

leaf and shoot passive diffusion

unknown

Sand‐Jensen et al. 1992

1

Brassicaceae

Barbarea stricta Andrz.

Emergent/Terrestrial

x

x

leaf and shoot passive diffusion

unknown

Sand‐Jensen et al. 1992

1

Brassicaceae

Cardamine amara L.

Emergent/Terrestrial

x

x

leaf and shoot passive diffusion

unknown

1

Campanulaceae

Lobelia dortmanna  L.

Submerged/Emergent

x

x

root passive diffusion

99.00%

Sand‐Jensen et al. 1992 Wium‐Andersen 1971; Richardson et al.  1984

Cyperaceae

Schoenoplectus tabernaemontani  (C.C. Gmel.) Palla

Emergent

x

x

root passive diffusion