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An Ecophysiological Approach to Quantifying Nitrogen Fixation by Lobaria Oregana

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An Ecophysiological Approach to Quantifying Nitrogen Fixation by Lobaria Oregana The Bryologist 107(1), pp. 82 87 Copyright q 2004 by the American Bryological and Lichenological Society, Inc. An Ecophysiological Approach to Quantifying Nitrogen Fixation by Lobaria oregana MARIE E. ANTOINE Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331, U.S.A. e-mail: [email protected] Current address: Department of Biological Sciences, Humboldt State University, Arcata, CA 95521, U.S.A. Abstract. Lobaria oregana is an epiphytic macrolichen associated with old-growth Douglas- ®r forests in the Paci®c Northwest. Nitrogen ®xation by this often-abundant cyanolichen provides an ecologically signi®cant input of new N to the forest ecosystem. This study estimates annual N2 ®xation by L. oregana using a model based on physiological ®eld measurements and laboratory experiments. Meteorological data from the Wind River Canopy Crane site and the H. J. Andrews Experimental Forest are used to calculate annual N2 ®xation rates, assuming that hydration and temperature are the two parameters controlling nitrogenase activity. At the crane site, estimated 21 annual N2 ®xation is 1.5 kg ha . In the H. J. Andrews Experimental Forest, L. oregana may ®x 21 21 2.6±16.5 kg N2 ha yr depending on its stand-level canopy biomass. The model's predictions are checked by using published growth rates and standing L. oregana biomass estimates to cal- culate independent values for annual N2 ®xation at each site. Keywords. Cyanolichens, Lobaria oregana, nitrogen ®xation, old-growth lichens. Cyanolichens dominate epiphyte assemblages in with meteorological data to model N2 ®xation. This wet old-growth, mid-elevation Douglas-®r forests approach was used to estimate annual N2 ®xation of Oregon and Washington (Neitlich 1993; Pike et by L. oregana at the canopy crane site in the Wind al. 1975; Sillett 1995). They are important ecosys- River Experimental Forest and at the HJA. The tem components because of their ability to ®x at- model's predicted values were compared to esti- mospheric N2 into forms of N available for plant mates of annual N2 ®xation that were calculated uptake (Denison 1979). Nitrogen is tightly con- independently from data on growth rates and stand- served in old-growth forests (Sollins et al. 1980), level biomass. and biological N2 ®xation brings new N into the ecosystem. Nitrogenous leachates (Millbank 1982) METHODS and in situ decomposition of cyanolichens (Rhoad- Study organism. Lobaria oregana is a foliose cyanoli- es 1983) supports canopy food webs (Carroll 1979). chen whose yellow-green thalli drape over branches or Decomposition of litterfall releases N to plants on grow loosely appressed to bark. It is one of only 3±4% the forest ¯oor (Pike 1978). of lichens representing a tripartite symbiosis among a my- Lobaria oregana (Tuck.) MuÈll. Arg. is the most cobiont (Ascomycota), a green algal photobiont (Chloro- phyta, Myrmecia), and a cyanobacterial photobiont (Nos- abundant N2-®xing lichen in these forests, often ac- toc) (Honegger 1991). Lobaria oregana is most accurately counting for 60±80% of the total epiphytic lichen referred to as a cephalodiate chlorolichen because the cy- biomass (McCune 1994; Pike et al. 1977; Sillett anobacterium is restricted to cephalodia, and the green 1995). Studies undertaken in the H. J. Andrews Ex- alga does the bulk of CO2 ®xation. perimental Forest (HJA) during the 1970's estimate Study site. Lobaria oregana was collected and ®eld- work conducted at the Wind River Canopy Crane 21 21 that L. oregana may ®x up to 4.5 kg N2 ha yr (WRCC) Research Facility near Carson, Washington. The (Denison 1979; Pike 1978), over 50% of the annual crane site is located within the Wind River Experimental new N input to the forest's nutrient budget (Sollins Forest (458499 N, 1218559 W) in the Gifford Pinchot Na- et al. 1980). No further attempts to quantify N ®x- tional Forest. The 4-ha crane plot is centered on a Liebherr 2 550 HC construction crane. The crane is 87 m high, has ation by cyanolichens in Douglas-®r forests have a horizontal reach of 85 m, and provides access to 105 m3 been made since these initial estimates. of old-growth forest canopy. The dominant canopy trees The objective of this study was to quantify an- are Pseudotsuga menziesii (Mirb.) Franco and Tsuga het- nual N ®xation by L. oregana. Field measurements erophylla (Raf.) Sarg.; Thuja plicata Donn. is also com- 2 mon. Stand age is approximately 500 years, and the site and laboratory experiments were conducted in or- displays classic old-growth characteristics (Franklin & der to identify which parameters in¯uenced N2 ®x- Spies 1991). The non-vascular epiphyte community is ver- ation rates, and these parameters were combined tically strati®ed, with peak abundance of L. oregana oc- 0007-2745/04/$0.75/0 2004] ANTOINE: NITROGEN FIXATION 83 curring in the ``light transition zone'' of the middle canopy ment. Thalli were placed upon saturated sponges in a tray (McCune et al. 1997). of distilled water, and then misted at 5-min. intervals using Sampling protocol. Lobaria oregana was collected at a spray bottle. Thallus water content (WC) was expressed two-month intervals during winter and spring of 2000 and in absolute terms, and the ``sacri®cial'' method was used 2001 as well as fall of 2000. During each sampling trip, to correct mass to an oven-dried basis (McCune et al. the canopy crane was used to access collection sites at 1996). two heights (ca 13 and 35 m) on two individuals each of A laboratory-based temperature response curve for ni- P. menziesii, T. heterophylla, and T. plicata. Different trogenase activity was constructed using lichens collected trees were utilized on each sampling trip. Three thalli were in spring 2001. Thalli were re-hydrated for 60 min. at taken from each site, for a total of 36 thalli per sampling temperatures from 0±208C. Nitrogenase activity was mea- trip. sured at each 28C interval (n 5 3 per temperature level). Physiological measurements. Nitrogenase activity PAR levels were kept constant at 100 mEm22 sec.21 dur- was measured using the acetylene reduction assay (ARA) ing re-hydration and subsequent ARAs. (Hardy et al. 1973). Acetylene was generated by reacting The relationship between thallus WC and nitrogenase calcium carbide with water, then injected into 300-ml air- activity was determined using lichens collected in fall tight Plexiglass incubation chambers to a concentration of 2000. First, thalli were re-hydrated for 0, 5, 10, 30, 60, 10% by volume. The chambers were shaken vigorously, 120, and 180 min. (n 5 3 per hydration time) to determine vented to atmospheric pressure, and internal 12-V fans how fast re-hydration occurred. Next, thalli were hydrated were engaged. Lichen thalli were incubated for 60 min., using carefully timed periods of misting and air-drying to and empty control chambers were used to quantify back- achieve 300, 250, 200, 150, 100, and 50% WC (actual ground levels of C2H4 present in the C2H2. After the in- WC was typically 620% of target). Nitrogenase activity cubation period, syringes were used to withdraw three 1- was measured for each WC (n 5 6 per level). Temperature ml gas samples from each experimental and control cham- and PAR were kept constant at ca 138C and 100 mEm22 ber. The samples were immediately injected into septum- sec.21, respectively. topped autosampler vials in order to ensure leak-proof Modeling N2 ®xation. The model rested upon the fol- transport back to the laboratory. Ethylene content of each lowing set of simplifying assumptions derived from re- sample was determined using a Varian model 330 gas sults of the ®eld measurements and laboratory experi- chromatograph equipped with a 0.318 3 76 cm stainless ments summarized above. 1) All thalli had to be hydrated steel column of Poropak N and a ¯ame ionization detector. to be physiologically active. 2) Rainfall immediately hy- drated and activated all thalli. 3) When rain stopped, all The theoretical 4:1 conversion ratio between C2H2 reduc- thalli stayed hydrated and active for 60 min. 4) N ®xation tion and N2 reduction rates was used (Crawford et al. 2 2000). was independent of canopy position and host tree species. Field measurements. The ARA was used to measure 5) N2 ®xation was not limited by light. 6) N2 ®xation rates nitrogenase activity in each of the 36 Lobaria oregana were controlled by temperature. thalli collected per sampling trip. These measurements Temperature-dependent N2 ®xation rates (nmol N2 per were made on the ground under ambient conditions that kg dry mass of lichen) were generated for each 30-min. approximated temperature and photosynthetically active period in the meteorological datasets. Daily, monthly, or radiation (PAR) recorded at the lichen collection site. PAR annual N2 ®xation was simply the sum of all 30-min. pe- was measured with the External Quantum Sensor on a riods in which L. oregana was hydrated. Rates were LiCor 6400 Portable Photosynthesis System. A digital scaled up to the stand level using the estimated canopy thermometer was used to measure temperature inside the biomass of L. oregana. At WRCC, standing biomass was 21 incubation chamber before and after the ARA, and di- approximately 550 kg ha (McCune et al. 1997). Esti- mates were made for sites within HJA where L. oregana rectly outside the chamber at 20 and 40 min. during the biomass was approximately 3,523, 2,620, 1,587 (Neitlich incubation. These ambient conditions were not intended 1993), and 500 kg ha21 (Denison 1979). to represent the entire day, or the entire season. Rather, The WRCC meteorological data used to drive the mod- the ®eld ARA were intended to capture ``snapshots'' of el were recorded at an open meteorological station on the nitrogenase activity in hydrated lichens under certain tem- ground near the crane tower.
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