Populus Fremontii) Seedling Growth and Survival

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Western North American Naturalist

Volume 72 Number 3 Article 6

11-5-2012

Inundation depth, duration, and temperature influence rF emon cottonwood (Populus fremontii) seedling growth and survival

L. C. Auchincloss University of California, Davis, CA, [email protected]

J. H. Richards University of California, Davis, CA, [email protected]

C. A. Young Stockholm Environment Institute, Davis, CA, [email protected]

M. K. Tansey Bureau of Reclamation, Sacramento, CA, [email protected]

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Recommended Citation Auchincloss, L. C.; Richards, J. H.; Young, C. A.; and Tansey, M. K. (2012) "Inundation depth, duration, and temperature influence rF emon cottonwood (Populus fremontii) seedling growth and survival," Western North American Naturalist: Vol. 72 : No. 3 , Article 6. Available at: https://scholarsarchive.byu.edu/wnan/vol72/iss3/6

This Article is brought to you for free and open access by the Western North American Naturalist Publications at BYU ScholarsArchive. It has been accepted for inclusion in Western North American Naturalist by an authorized editor of BYU ScholarsArchive. For more information, please contact [email protected], [email protected]. Western North American Naturalist 72(3), © 2012, pp. 323–333

INUNDATION DEPTH, DURATION, AND TEMPERATURE INFLUENCE FREMONT COTTONWOOD (POPULUS FREMONTII) SEEDLING GROWTH AND SURVIVAL

L.C. Auchincloss1,4, J.H. Richards1, C.A. Young2, and M.K. Tansey3

ABSTRACT.—Fremont cottonwood (Populus fremontii) is an early successional foundation species found in riparian forest ecosystems in the North American Southwest. Along rivers, the upper limit of the seedling establishment zone depends on the proximity of seedling roots to the declining water table. The lower limit is a function of the maximum elevation of inundation or scour. Fremont cottonwood seedlings are likely to experience short-term (1- to 5-week) inundation during their first year of growth under both natural and human-influenced hydrologic regimes. Previous studies show that inundation can account for more than 70% of seedling mortality during this time. Using controlled inundation experiments, we found that seedlings of Fremont cottonwood have high tolerance of inundation to the soil surface and a reasonable tolerance of complete shoot submergence for a duration of 1 or 2 weeks (22% and 50% mortality, respectively). Mortality increased linearly with days of complete submergence (mortality percentage = 4.6 + [2.5 × days of submergence]). Warm water temperature (25/18 °C day/night) during complete submergence adversely affected seedling biomass and survival, resulting in 64% mortality versus 39% with cooler water temperatures (18/11 °C day/night). Our results indicate that establishment of new Fremont cottonwood populations in the riparian corridor will be more successful when flows do not completely cover the shoots of seedlings for more than 2 weeks and if water temperatures during inundation are cool. From the perspective of the management of river flows for cottonwood recruitment, deep, prolonged, late-season (warm water) inundations are the most detrimental.

RESUMEN.—El álamo negro (Populus fremontii) es una especie de sucesión temprana en los ecosistemas de bosques ribereños, en el suroeste norteamericano. A lo largo de los ríos, el límite superior de la zona de establecimiento de plántulas depende de la proximidad de las raíces de las plántulas al nivel freático decreciente. El límite inferior es una función de la elevación máxima de inundación o abrasión. Es posible que las plántulas de álamo negro experimenten una inundación de corto plazo (de 1 a 5 semanas) durante sus primeros años de crecimiento en sistemas hidrológicos naturales y con influencia humana. Estudios anteriores revelaron que la inundación puede explicar más del 70% de la mortalidad de las plántulas durante este tiempo. Mediante experimentos de inundación controlada, encontramos que las plántulas de álamo negro poseen una elevada tolerancia a la inundación de la superficie del suelo y una tolerancia razonable a la inmersión completa del tallo durante una o dos semanas (22% y 50% de mortalidad respectivamente). La mortalidad aumentó en forma lineal con los días de inmersión completa (porcentaje de mortalidad = 4.6 + (2.5 × días de inmersión). La temperatura caliente del agua (25/18 °C día/noche) durante la inmersión completa afectó de manera adversa la biomasa y la supervivencia de las plántulas, lo que resultó en un 64% de mortalidad contra el 39% en temperaturas más frías (18/11 °C día/noche). Nuestros resultados indican que el establecimiento de nuevas poblaciones de álamos negros en el corredor ribereño tendrá mayor éxito cuando los caudales no cubran por completo los tallos de las plántulas por más de dos semanas, y si la temperatura del agua es fría durante la inundación. Desde la perspectiva del manejo de los caudales de los ríos para el reclutamiento de álamos negros, las inundaciones profundas, prolongadas y en temporada tardía son las más perjudiciales.

Perennial plant species of semiarid riparian river stage and the beginning of recession ecosystems must tolerate a wide range of water coincide with seed dispersal and germination of conditions ranging from complete submer- riparian trees and shrubs on exposed sediments. gence to drought. Under natural conditions The regeneration of riparian forests depends semiarid riparian zones usually experience first on the ability of the seedlings to extract inundation early in spring followed by gradual sufficient water from root-zone sediments. It soil drainage and a decline of the water table also depends on their ability to keep up with a during the summer (Brinson et al. 1981, Koz - declining water table associated with the reces- lowski 2002, Stella et al. 2006). Early high- sion stage of the river hydrograph (Stromberg

1Department of Land, Air and Water Resources, University of California, Davis, CA 95616. 2Stockholm Environment Institute, 133 D Street, Davis, CA 95616. 3Bureau of Reclamation MidPacific Region, 2800 Cottage Way, Sacramento, CA 95825. 4E-mail: [email protected]

323 324 WESTERN NORTH AMERICAN NATURALIST [Volume 72 et al. 1991, Mahoney and Rood 1992, 1998, reexposed to high light, the potential for Scott et al. 1997, Kranjcec et al. 1998, Rood et oxidative damage to their leaves is high al. 2003). However, depending on the timing (Parolin 2009). Thus, physiological stress may of precipitation, snowmelt rate, dam releases, occur both during and after inundation and and other conditions, seedlings growing along can lead to plant mortality or decreased pro- rivers in spring and summer may be subject to ductivity. Damage and stress can result in short-term flooding (Mahoney and Rood 1998, plant death up to 2 weeks postinundation Amlin and Rood 2001). Thus, regeneration of (Banach et al. 2009). riparian forests depends also on the ability of Considering the stresses and plant acclima- seedlings to survive temporary inundation. tion potential, the severity of physiological This study examines the effects of floodwater effects of inundation on cottonwood seedlings conditions and plant age on the growth and depends on several environmental factors: survival of Fremont cottonwood (Populus fre- duration of inundation, depth of inundation, montii S. Watson ssp. fremontii) seedlings. developmental age of the plant, and water Riparian Fremont cottonwood occurs from temperature during inundation. Hosner (1958, western Texas through New Mexico, Arizona, 1960) observed that complete submergence California, Nevada, and Utah. In mature ripar- for 16 days negatively impacted the survival of ian forests, it is a foundation species, making cottonwood seedlings (among other riparian up a large portion of the biomass and influenc- species). Short-term shoot submergence of 2–4 ing the overall productivity of the ecosystem days led to partial leaf death, whereas 8-day (McBride and Strahan 1984, Warner and Hen- submergence required complete renewal of drix 1984, Stromberg 1993, Rood et al. 2003). the leaf canopy. Sixteen-day submergence led Along the Sacramento River, California, Fre- to death of all seedlings of plains cottonwood mont cottonwood disperses seed that germi- (Populus deltoides; Hosner 1958). A later study nates within 2 days on exposed substrates in from Amlin and Rood (2001) showed that cut- April–May. This seed dispersal is coincident tings of 3 cottonwood species (P. angustifolia, with monthly average peak flows (prior to dam P. balsamifera, and P. deltoides) survived more regulation) of the river’s major tributaries, the than 7 weeks of inundation to the soil surface, Feather and American rivers (USGS 2010a, although dry weight was lower in inundated 2010b). Because Fremont cottonwood estab- treatments compared to controls. lishes close to the river’s edge on exposed Although these studies examined flooding point bars and germinates early in spring, the for different durations, they did not compare seedlings are likely to experience brief inun- the effects of inundation to the soil surface and dation due to either natural or human-induced complete shoot submergence. Complete inun- hydrologic changes. In some years, inundation dation of the shoot is expected to be more has accounted for more than 70% of seedling damaging than partial inundation of the soil mortality during the first year of growth along and stem base. This is because an inundated the Sacramento River (Morgan 2005). shoot has little or no access to the atmosphere, Flood events can cause damage to estab- a condition that hinders internal oxygen trans- lishing seedlings through several processes, port and inhibits photosynthesis (Kozlowski including substrate saturation and root hypoxia, 2002). Also, the described experiments were inhibition of photosynthetic carbohydrate gen- conducted with warm, still water and may not eration, erosion of sediments or plants, and be representative of inundation by cool, flow- burial by sediments. Physiological damage ing river waters that contain higher dissolved during inundation includes suppressed shoot oxygen concentrations. It is important to rein- and root growth, delayed leaf formation, accel- vestigate this topic, as inundation with warm, erated senescence, and root decay (Kozlowski stagnant water decreased growth of some 2002). These stresses become more pro- riparian species to a much greater extent than nounced as the duration of inundation increases inundation with cool, flowing water (Brink (Neuman et al. 1996). Complete inundation of 1954, Kozlowski 2002). shoots inhibits photosynthesis, and warm water Most work on inundation of cottonwood temperature during inundation increases res- has been done with cuttings (e.g., Amlin and piration rate and depletion of carbohydrates. Rood 2001). To study establishment of new After submergence ends and seedlings are populations we need to consider the effect of 2012] FLOOD SURVIVAL OF COTTONWOOD SEEDLINGS 325 inundation on seedlings because of their small Cache Creek, Yolo County, CA) was used. This size, younger developmental age, and lack of soil was a good match to previous particle size nutrient and carbohydrate reserves. Plant age and soil profile data from a point bar at RM affects stem and taproot size, which affects the 192.5 on the Sacramento River where Fremont potential amount of stored nutrients and car- cottonwood establishment occurs. Seeds from bohydrates and, thus, affects the plant’s ability 11 high-germination (78%–100%) trees were to withstand long inundation duration. Seed - sown on the sandy soil in 240 large, approxi- ling establishment is particularly important in mately 650-mL Deepots® (Stuewe & Sons, natural ecosystems that are subject to flooding Inc., Tangent, OR) on 18 June 2008; 5 seeds stress. Thus, it is important to investigate the were sown per pot. After germination, seed - specific tolerance of P. fremontii seedlings to lings were thinned to one seedling per pot. inundation, considering that the species is a Seedlings were maintained outdoors on the foundation species along many western water- University of California, Davis (UC Davis) ways. Large differences in flood response campus, elevation 16 m asl, with a constant physiology and growth rate are known to exist water table 10–15 cm below the soil surface, among 13 hybrid poplar genotypes resulting and they were fertilized daily by top watering from crosses between P. trichocarpa, P. nigra, with 5% modified Hoagland’s solution (Epstein P. deltoides, and P. euramericana (Guo et al. and Bloom 2005) until treatments com- 2011). Because large differences existed among menced. One month later seed was sown in these hybrids, differences in flooding toler- 240 small, approximately 165-mL Conetainers® ance may vary significantly among species, (Stuewe & Sons, Inc., Tangent, OR), and seed- and we cannot necessarily apply results from lings were grown with the same procedures examination of other species to P. fremontii. described above. The 2 sowing dates provided In this experiment, we examined the effects seedlings of different age at the beginning of of water temperature, duration of inundation, the experimental treatments. and depth of inundation on Fremont cotton- Experimental Design and Treatments wood seedlings of 2 ages. We tested the hypothesis that warmer inundations of longer Three pairs (blocks) of insulated galvanized duration and greater depth would result in steel stock tanks (0.6 × 0.6 × 1.2 m, 432 L) decreased growth and survival of seedlings. were filled with deionized water. Racks hold- We also examined 2 ages of Fremont cotton- ing the plants were placed at different depths wood seedlings to test the hypothesis that more- to allow complete submergence of the plant developed plants, presumably with greater shoots or submergence just to the soil surface. nutrient and carbohydrate stores, are better Control plants blocked with each pair of tanks able to withstand inundation. The results from were grown with a constant water table 12.5 this study provide characterization of multiple cm below the soil surface. We used a thermo- water conditions important for cottonwood statically controlled cooling unit to regulate seedling survival of inundation and hence for the temperature of the cool treatment tanks. the establishment of new populations and Cool treatment tanks (one from each pair) maintenance of semiarid riparian ecosystems. were set to oscillate between 11 °C at night and 18 °C during the day. This regime approxi- METHODS mated Sacramento River water temperature during summer 2004–2006. Warm tanks oscil- Seedling Germination and Plant Growth lated naturally with diurnal temperature change In May 2008, catkins were collected from from 18 °C at night to 24 °C during the day. 13 trees between river mile (RM) 190 and 220, Water was circulated within each tank via a elevation 33–52 m asl, of the Sacramento submersible pump to simulate flowing river River, California. Seeds were cleaned and water, to maintain water oxygenation, and to stored with desiccant at 4 °C, similar to maintain uniform temperature throughout. Segelquist et al. (1993). Germination tests The experimental design was a split-split- were conducted on moistened filter paper at plot randomized complete block. Within the 3 approximately 20 °C. A commercially available blocks, plants were randomly assigned to sandy soil (Schwartzgruber plaster mix mined treatments with 4 (occasionally 2–3) plants per from a tributary of the Sacramento River, treatment per block (Table 1). Control plants 326 WESTERN NORTH AMERICAN NATURALIST [Volume 72

TABLE 1. Number of plants within each inundation treatment (Total) and number of plants harvested at each time point: (a) immediately after inundation ended (post inund) or (b) after 4 weeks of recovery without inundation (post rec). Four young and 4 old seedlings were harvested for initial biomass just before inundation treatments were applied. The structure of treatments at the left and along the top row is representative of the structure of each block: inundation levels and durations were randomized within plant ages, which were randomized within tanks of warm or cool water (3 replicates each). The numbers in this table represent plants harvested from all 3 blocks, generally 4 plants of each treatment within each block for a total of 12 plants. Seedling survival during germination sometimes limited this number.

______1-week inundation ______2-week inundation ______4-week inundation Inundation Post Post Post Post Post Post Temp. Age level Total inund rec Total inund rec Total inund rec Warm Young none 4 0 4 11 4 7 6 0 6 soil surface 12 4 8 12 4 8 12 4 8 complete 12 4 8 12 4 8 12 4 8 Old none 0 0 0 6 0 6 11 4 7 soil surface 0 0 0 9 3 6 9 3 6 complete000 1046 936 Cold Young none 4 0 4 12 4 8 8 0 8 soil surface 12 4 8 12 4 8 10 4 6 complete 12 4 8 11 4 7 10 4 8 Oldnone000 606 936 soil surface 0 0 0 9 3 6 9 3 6 complete000 1046 936 were paired with treatment plants for final vest, plant containers were removed from harvests and for some intermediate harvests. treatments and allowed to drain. Plant shoots The variables for each treatment were (A) age were cut at the root collar and placed in of the plant: 6 or 10 weeks old at time of inun- deionized water in a zipper-lock plastic bag. dation; (B) temperature of inundation: cool or The pot, soil, and plant roots were also sealed warm; (C) duration of inundation: 1 week (6- in plastic bags, and all samples were stored at week-old plants only), 2 weeks, or 4 weeks; 4 °C until processed. and (D) depth of inundation: soil surface, com- Total leaf area and stem length for each plete submergence (all aerial portions of the plant were determined by scanning all leaves plant covered), or no inundation (control with and stems within 3 days of harvest. Scans were constant water table 12.5 cm below the soil analyzed using custom macros in Image J surface). The main plot was temperature with (National Institutes of Health; http://rsb.info plant age randomized as a subplot and depth .nih.gov/ij/). Roots were dissected from the and duration randomized as sub-subplots. soil to best maintain overall root structure. Each plant was placed in an inundation tank Root samples from each plant were washed corresponding to its block and its inundation with deionized water, placed in vials, and temperature treatment assignment. Inunda- stored in a refrigerator until they could be tion tanks were outdoors at the UC Davis scanned. Roots were scanned and measure- campus and received full morning and midday ments of total root length and average diame- sunlight for approximately 10 h and afternoon ter were made using standard procedures for shade for 4 h. Inundation treatments com- the program WinRhizo 2003B (Regent Instru- menced on 26 August 2008, and the experiments, Inc., Nepean, Ontario, Canada). The ment ended 8 weeks later. roots, leaves, and stem of each plant were dried at 45 °C for 3 days, and dry weights Harvests and Measurements were recorded. At the end of each inundation period, 1 Statistical Analyses plant (occasionally 2 plants) from each treatment and block was harvested, and 2 or 3 Contingency table analyses of survival were were elevated to the level of controls and performed using total levels of mortality after allowed to recover for 4 weeks prior to final inundation and recovery (Glantz 2002). This harvest. Plants within treatment combinations cumulative survival analysis provided a realis- within blocks were subsamples. At each har- tic assessment of the effect of inundation. If a 2012] FLOOD SURVIVAL OF COTTONWOOD SEEDLINGS 327

Fig. 1. Percent mortality comparing treatment factors: (a) inundation depth, (b) water temperature (warm: 25/18 °C day/night; cool: 18/11 °C day/night), and (c) plant age (upon inundation: younger seedlings = 6 weeks, older seedlings = 10 weeks). Values and analyses depicted in panels b and c refer to plants in the complete inundation treatment only. Bars with different letters (A and B) indicate significant differences based on contingency analyses; see text for P values associated with each comparison. plant was alive immediately after inundation RESULTS but had been damaged or stressed so that it Mortality could not recover, it was inferred that inundation caused mortality, as no control plants died Contingency table analyses of cumulative during the 4-week recovery period. Regres- mortality of Fremont cottonwood seedlings sion analysis using SigmaPlot (Systat Software, during the inundation and 4-week recovery Inc., San Jose, CA) was performed to assess period provided a clear assessment of the plant mortality over time. ANOVA analyses overall effects of inundation. These analyses using SAS (SAS Institute, Inc., Cary, North showed that seedling death varied with depth Carolina) were performed for the split-split- of inundation, inundation water temperature, plot design using Proc GLM. Factors associ- and duration of inundation. Across all treat- ated with higher-level plots (main plots and ments, completely submerged plants suffered subplots as opposed to subplots and sub-sub- approximately 5-fold greater mortality (51%) plots, respectively) generally have higher lev- than noninundated control plants and plants els of variance and must be tested using larger inundated to the soil surface (plants in both- error terms. Thus, analysis of the main plot, treatments experienced <10% mortality, P < temperature, was performed with the larger 0.00001; Fig. 1a). Plants inundated to the soil error term block × temperature and the analysis surface suffered little mortality and did not of subplots with block × temperature × age. differ from controls (P = 0.98). Within the The analysis of the effect of the sub-subplot complete submergence treatment, plants in inundation level used the smallest error term warm water had significantly greater mortality (block × inundation level × temperature × than plants in cool water across all treatments age). By specifying these error terms, we could (P = 0.02; Fig. 1b). Both young and old compare the effects of temperature, age, depth seedlings had high mortality in the complete of inundation, and the interactions among submergence treatment across all durations of these factors using Proc GLM in SAS 9.2. inundation (P = 0.38; Fig. 1c). 328 WESTERN NORTH AMERICAN NATURALIST [Volume 72

Mortality was linearly related to duration of inundation (% mortality = 4.60 + [2.54 × days of submergence]; P = 0.024, Adj. R2 = 0.93; Fig. 2), consistent with results of contingency table comparisons among the specific treatments. Plants completely submerged for 4 weeks showed significantly greater mortality (71%) than plants inundated for either 1 week (22%, P = 0.001) or 2 weeks (50%, P = 0.02). All plants suffering mortality after complete submergence for 4 weeks were dead upon removal from inundation, with the exception of 2 plants that died within 5 days during the recovery period. Approximately 75% of plants that died as a result of 2 weeks of complete submergence were dead upon removal from inundation. The other 25% of plants died within a week of removal. Within young plants Fig. 2. Linear relationship between average percent exposed to complete submergence for 1 week, mortality and days of complete inundation. approximately half of the plants suffering

Fig. 3. Total plant biomass of surviving plants comparing treatment factors: (a, d) inundation depth, (b, e) inundation duration, and (c, f) water temperature within younger (a, b, c) and older (d, e, f) plants. Letters (A and B) indicate significant differences (P < 0.00001) based on ANOVA. Error bars represent one standard error around the mean. Note different scales for younger and older plants. 2012] FLOOD SURVIVAL OF COTTONWOOD SEEDLINGS 329

Fig. 4. Average root length density in full rooting volume per plant (a, b) and average root diameter (c, d) from harvests immediately after 2-week (a, c) or 4-week (b, d) inundation periods and for different inundation treatments. Older and younger seedlings were compared separately because of large differences in sample size due to mortality. Bars with different letters (A, B, C and R, S) indicate differences with given P values based on ANOVA. Error bars represent one standard error around the mean. mortality were dead upon removal from inun- among treatment durations within the com- dation and half died within a week of removal. plete submergence treatment (Fig. 3b, 3e). Among young plants only, no statistical differ- Also, cool water temperature resulted in much ence in mortality was observed when they higher average biomass after complete sub- were completely submerged for 1 week or 2 mergence and recovery; however, very few weeks (P = 0.20). plants surviving for this analysis meant P = 0.11. (Fig. 3c, 3f). Biomass of Surviving Plants Biomass measurements were analyzed only Root Characteristics Immediately for living individuals that survived both the After Inundation inundation and recovery periods. After inun- Few differences were observed in root length dation and recovery, both younger and older per plant and average root diameter immedi- seedlings that were completely submerged ately after the 2-week inundation period, when had less than one-third the biomass of compa- surviving plants of different ages exposed to rable control, noninundated plants. They also different inundation durations (Fig. 4a, 4c) were were smaller than plants in the soil-surface compared. Younger plants subject to complete inundation treatment (P < 0.0001; Fig. 3a, 3d). submergence had approximately half the aver- However, plants inundated to the soil surface age root length compared to plants subject to and controls did not show a significant differ- control conditions or soil-surface inundation; ence in biomass (P = 0.83). Neither older nor this difference was nearly significant but the younger plants were different in biomass test had low power because of limited survival 330 WESTERN NORTH AMERICAN NATURALIST [Volume 72 in this treatment (P = 0.075, power = 0.354; ration. Anaerobic respiration is only about Fig. 4a). After the 4-week inundation period, 20% as efficient as aerobic respiration and larger and significant differences were ob - produces toxic compounds, which can damage served, despite small numbers of surviving tissues (Roberts et al. 1984, Neuman et al. plants. Both younger and older plants dis- 1996, Kozlowski 2002). Also, when stored car- played a consistent pattern of greatly reduced bohydrate supplies become limited, the plant root length and increased average diameter, no longer has resources to maintain organs, indicating more fine-root loss for complete especially fine roots, which then die and inundation plants compared to controls (Fig. decompose. This compromises the ability of 4b, 4d) or soil-surface innundated plants. the root system to absorb nutrients and water not only during inundation but after the shoot DISCUSSION is reexposed to the atmosphere (Borman and Larson 2002, Kozlowski 2002, Banach et al. This study aimed to characterize multiple 2009). Lower root length per plant and higher water conditions important for Fremont cot- average root diameter in the complete sub- tonwood seedling survival of inundation and mergence treatment immediately after the 4- hence for establishment of new populations week inundation period are consistent with along the Sacramento River and other water- the hypothesis that fine roots die and decom- courses. We evaluated the relative importance pose during 2- and 4-week inundation periods of the key environmental factors: inundation (Fig. 4). The death of the fine roots would depth, inundation duration, and water tem- increase average diameter. Likewise, both perature. Differences in response to these fac- growth inhibition of roots and death of fine tors were relatively small among first-year roots would decrease overall root length. seedlings of different age. Inundation depth, Longer duration of complete submergence duration, and water temperature all signifi- resulted in a linear increase in plant mortality cantly affected survival and health of Fremont (Fig. 2). This again is consistent with the cottonwood seedlings. The combination of hypothesis that waning carbohydrate stores environmental factors most detrimental to and accumulation of toxic compounds con- seedling health was complete submergence of tributed to seedling death, since we would seedlings in warm water for long duration (4 expect stored carbohydrates to be broken weeks). Negative effects of this treatment down over time as they are used to support combination were apparent as reduced sur- respiration. Once carbohydrate stores are vival (Fig. 1) and, for surviving plants, reduced depleted, plants are unable to maintain nor- biomass and root length (Figs. 3, 4). mal metabolic activity and growth, eventually leading to plant death (Roberts et al. 1984, Complete Inundation Neuman et al. 1996, Kozlowski 2002). It is Consistent with results from Hosner’s unclear whether shorter inundation periods of (1958) experiment examining cottonwood 1 and 2 weeks showed a difference in mortal- seedlings, complete submergence of the shoot ity. Fine-scale determination of the effects of was deleterious for Fremont cottonwood short-term submergence will require larger seedling survival and growth over all ages, sample sizes. temperatures, and durations. Energy limita- Adding to previous knowledge of cotton- tion via inhibition of photosynthesis, depletion wood inundation response, we found that sur- of carbohydrates, accumulation of toxic com- vival, growth, and recovery of seedlings were pounds, and subsequent root decay may all adversely affected by warm water (Figs. 1, 3). have contributed to the mortality, as well as to Higher mortality with warm water inundation the reduced growth of surviving plants of Fre- and lower mortality with cool water suggests mont cottonwood under complete submer- that the slope of the average relationship given gence (Roberts et al. 1984, Neuman et al. in Fig. 2 could be adjusted to model effects of 1996, Borman and Larson 2002, Kozlowski different water temperatures. The detrimental 2002, Banach et al. 2009). With the shoot com- effect of complete warm water inundation was pletely submerged, photosynthesis and growth likely due to higher respiration rates, which are inhibited, and oxygen limitation requires would have depleted carbohydrate stores faster all tissues of the plant to use anaerobic respi- than the lower respiration rates in cool water. 2012] FLOOD SURVIVAL OF COTTONWOOD SEEDLINGS 331

An alternative hypothesis of post-inunda- Applications tion stress caused by reexposure of leaves to These findings can be used in developing high light conditions (Parolin 2009) is not con- river management strategies and riparian for- sistent with the observations in our experi- est restoration plans. The results suggest that ment. Most plants that did not survive were only seedlings with partial or complete shoot dead at the beginning of the recovery period; system submergence will show negative effects if post-inundation stress was important, mor- after short-term (2- to 4-week) inundation. tality should have occured later. Furthermore, Therefore, restoration efforts and river man- results for root length per plant and average agement should aim to develop new popu- diameter (Fig. 4) suggest effects during and lations of Fremont cottonwood seedlings in not after inundation. These results support the areas that will experience only abbreviated hypothesis that fine-root death and decay oc - shallow inundation. To the extent river stage curred during the inundation period. Neverthe- can be managed, flow regimes that minimize less, analyses of soluble carbohydrates before inundation when seedling shoots are short and and after inundation would be needed to fully more vulnerable would promote survival. assess the carbohydrate depletion hypothesis. Inundation of longer than 2 weeks should be Inundation to the Soil Surface avoided to ensure good seedling survival, especially when warmer water temperatures Inundation to only the soil surface did not prevail. The cool temperature treatment in this affect Fremont cottonwood seedling survival experiment approximated the in-stream sum- or biomass accumulation after recovery in this mer temperatures of the Sacramento River in experiment. These results are consistent with the reach between Red Bluff and Colusa. For Amlin and Rood’s (2001) investigation of Popu- this reach, water temperature is influenced lus cuttings, which found reasonable tolerance mainly by daily air temperature. However, of 3 cottonwood species to 7-week soil inunda- water temperature in other riparian systems tion. Our results indicate that seedlings are may be significantly impacted by human activ- likely to survive soil-surface inundation peri- ities or upstream riparian vegetation. ods longer than 4 weeks, similar to cuttings, In other riparian systems, releases of warm because we saw no significant detrimental water from reservoirs, as well as embayments effects to biomass of seedlings inundated to that reduce flow rate, can result in warming of the soil surface compared to controls. Because river water temperatures. Likewise, water the shoot system was still in contact with the withdrawals and channel engineering can atmosphere, the plants in our study were able warm river waters by reducing the assimila- to continue growth during the 4-week inunda- tive capacity of the river for heat and by tion period, with the result that their ending reducing the potential for groundwater buffer- biomass was not significantly different from ing of temperature (Poole and Berman 2001). control plants (Fig. 3). Mature cottonwoods Riparian forests themselves can contribute to form shallow adventitious roots and lenticels maintaining cooler water by providing shade along the stem to facilitate oxygen exchange or slowing heat exchange, thus reducing tem- under partially or fully inundated soil condi- peratures of the surface and groundwater tions (Pereira and Kozlowski 1977, Nilsen and adjacent to the stream (Larson and Larson Orcutt 1996). Although the seedlings in our 1997, Poole and Berman 2001). However, this experiment were too small to form lenticels, temperature regulation is lessened as stream development of shallow root systems and channels widen with increased sediment ero- aeren chyma in roots may have contributed to sion from surrounding land and decreased survival and growth maintenance of roots flow power from damming, water diversion, despite the soil-surface inundation. Future and channel engineering. Wider channels can- experiments could examine longer inundation not be as well shaded and insulated as nar- periods for seedlings to determine if they have rower channels, and wide channels have less the same tolerance to flooding as the cuttings capacity for temperature buffering (Poole and examined in Amlin and Rood’s study (2001). Berman 2001). On the basis of our results, sig- They could also quantify the length of time nificant changes to water regime could seedlings can be exposed to soil-surface flood- increase water temperatures and potentially ing without deleterious effects. decrease seedling survival. If riparian forests 332 WESTERN NORTH AMERICAN NATURALIST [Volume 72 die and fail to regenerate, water temperatures LITERATURE CITED could further increase. This negative feedback condition would not only accelerate riparian ALLAN, J.D. 1995. Stream ecology: structure and function of running waters. Chapman & Hall, London, United forest decline but also contribute to detrimen- Kingdom. tal effects on associated aquatic communities AMLIN, N.A., AND S.B. ROOD. 2001. Inundation tolerances (Baltz and Moyle 1984, Barton et al. 1985, of riparian willows and cottonwoods. Journal of the Allan 1995, Poole and Berman 2001). American Water Resources Association 37:1709–1720. 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