Biol Invasions (2012) 14:2331–2342 DOI 10.1007/s10530-012-0232-y
ORIGINAL PAPER
Development and application of a UV attainment threshold for the prevention of warmwater aquatic invasive species Andrew J. Tucker • Craig E. Williamson James T. Oris
•
Received: 28 September 2011 / Accepted: 27 April 2012 / Published online: 11 May 2012 Ó Springer Science+Business Media B.V. 2012
Abstract Abiotic factors are important regulators of biological invasion and a recent study in Lake Tahoe (CA/NV, USA) showed that ultraviolet radiation (UV) can play a role in mediating warmwater fish invasion. In this study we highlight field and laboratory experiments that indicate strong species related differences in UV-induced stress between native and non-native fish species inhabiting the nearshore environment in Lake Tahoe. We use this differential UV sensitivity to develop a UV Attainment Threshold (UVAT) that if realized could be used to reduce susceptibility to warmwater fish invasion in nearshore environments. The UVAT is a target value for water transparency based on: (1) incident solar UV exposure levels during peak spawning season, and (2) experimentally derived UV exposure levels lethal to larval warmwater fish. We suggest that this value can be easily measured, monitored, and targeted to reduce the establishment and spread of invasive fish species. We also discuss how the UVAT increases the cost effectiveness of invasive species management. This approach could be relevant for any aquatic invasive species that is UV A. J. Tucker (&) C. E. Williamson J. T. Oris Department of Zoology, Miami University, 212 Pearson Hall, Oxford, OH 45056, USA e-mail:
[email protected] C. E. Williamson e-mail:
[email protected] J. T. Oris e-mail:
[email protected]
sensitive and constrained to relatively shallow water environments by, e.g. requirements for warmer spawning temperatures. Because many aquatic systems are threatened by both invasive species and declining water transparency we suggest that this research could have important applications in many systems, particularly in colder more UV transparent waters found in regions such as western North America. Keywords Ultraviolet radiation Abiotic factors Habitat invasibility Warmwater fish
Introduction Invasion by exotic species is a major concern in freshwater aquatic ecosystems (Richter et al. 1997; Dudgeon 2006), and poses a particularly grave threat to the persistence of native fish populations (Lassuy 1995). Yet considerable uncertainty remains concerning the most effective ways to prevent and manage biological invasion in inland waters (Enserink 1999; Williamson 1999). A central unresolved question is: what controls the suitability of habitats for invasion by exotic species? Traditionally the physical and biological characteristics of habitats that control the potential for exotic species to invade and establish have been viewed as components of an ‘‘invasion-window’’ (Johnstone 1986) or ‘‘niche opportunity’’ (Shea and Chesson 2002) that can be altered by disturbance. In
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freshwater ecosystems most natural and human disturbances that might open an invasion-window will also generate changes in water transparency. For example, transparency to visible light decreases with cultural eutrophication (Edmondson 1991; Seehausen et al. 1997) and with the introduction of planktivorous fish (Mazumder et al. 1990; Kaufman 1992). A recent report from Lake Tahoe, a large sub-alpine lake in western USA, demonstrated that water transparency to ultraviolet radiation (UV) can play a role in regulating the establishment of non-indigenous warmwater fish (Tucker et al. 2010). Invasive warmwater larval fish incubated in transparent high-UV sites experienced high mortality, while those incubated in turbid lowUV sites survived well. This finding is consistent with the emerging consensus that abiotic factors are important regulators of biological invasion (Holway et al. 2002; Dethier and Hacker 2005; Menke and Holway 2006; Gerhardt and Collinge 2007). Here we use Lake Tahoe as a case study to show how aquatic invasive species prevention and management strategies that focus on regulating water transparency, and thus UV exposure, could help to stem biological invasion in aquatic systems. This is an especially timely report for Lake Tahoe where non-native species appear to be replacing native minnows in the nearshore. Native fish density has declined over the last two decades lakewide (Ngai et al. 2011) and in the Tahoe Keys (a formerly important nursery habitat for native minnows and one of the few habitats where warmwater fish are well established in the lake), native minnow species have virtually been eliminated (Kamerath et al. 2008). Yet, many more aquatic systems are threatened by both invasive species and declining water transparency. Thus, this research could have important applications elsewhere and we suggest it has relevance for any aquatic invasive species that is UV sensitive and constrained to relatively shallow water environments by, e.g. requirements for warmer spawning temperatures. Experiments in eastern USA lakes have demonstrated that high UV transparency reduces the reproductive success of warmwater fish in shallow waters (Williamson et al. 1997; Huff et al. 2004; Olson et al. 2006). Lake Tahoe is much more transparent than these lakes. However, reductions in nearshore UV transparency may have provided a refuge for warmwater fish to successfully nest and to establish selfsustaining populations in Lake Tahoe. In fact, Lake
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Tahoe has experienced a gradual loss of water clarity in recent decades, with a decline in average annual Secchi transparency from 31 m in 1968 to 21 m by 1998 (Jassby et al. 1999). During this period a number of non-indigenous warmwater fish species (including bluegill, Lepomis macrochirus, and largemouth bass, Micropterus salmoides) have established populations in a limited number of nearshore locations (Reuter and Miller 2000). Data from nearhore-to-offshore UV profiling transects in Lake Tahoe show that shallow environments nearshore to some of the major inlets are far less UV transparent than offshore waters and that patterns of UV transparency change from month to month (Rose et al. 2009). This is important because during summer months shallow nearshore habitat is necessary to provide the warm temperatures that permit spawning by non-native species such as largemouth bass. In present day Lake Tahoe, native minnow species and introduced warmwater fish both inhabit the nearshore environment. However, the only well established non-native warmwater fish populations are limited to sites in the southern end of the lake (e.g. Tahoe Keys) that are characterized by extensive development and that are in close proximity to some of the lake’s largest tributaries (Kamerath et al. 2008). Water transparency at these sites tends to be lower than elsewhere in the lake and may explain the suitability of such sites for the establishment of nonnative fish populations (Tucker et al. 2010). Native minnows occur widely and in nearshore habitats with high levels of UV. In this study we highlight field and laboratory experiments that indicate strong species related differences in UV-induced stress for fish inhabiting Lake Tahoe. We use this differential UV sensitivity to develop a ‘‘UV Attainment Threshold’’ that if realized could reduce susceptibility to exotic centrarchid fish species establishment in nearshore Lake Tahoe. We present the results from experiments comparing the UV tolerance of native minnow (Lahontan redside, Richardsonius egregius) larvae with that of non-native warmwater fish (bluegill and largemouth bass) larvae (Fig. 1). We also present data from field surveys of UV and temperature in nearshore Lake Tahoe. From these data we develop a UV attainment threshold (UVAT) for 11 nearshore locations in Lake Tahoe. The UVAT is a target value for UV transparency based on, (1) surface UV exposure during peak spawning season, and (2)
Development and application of a UV
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Fig. 1 Yolk-sac larvae, a bluegill (L. macrochirus), b Largemouth bass (M. salmoides), and c Lahontan redside shiner (R. egregius). Note the greater density of photoprotective pigment in the native redside larva
experimentally derived UV exposure levels lethal to larval warmwater fish. For our purposes we present the UVAT as the % of 305 nm surface UV exposure that must penetrate to a given depth in order to prevent largemouth bass reproduction within a site. The UVAT emphasizes largemouth bass because they were the more UV tolerant of the two warmwater fish tested. Thus, water clarity improvements that prevent bass survival will also likely prevent bluegill reproduction. We suggest that this value can be easily measured and monitored with a profiling UV radiometer or modeled from water samples analyzed for transparency in the lab with a spectrophotometer, and used to manage nearshore
waters in an effort to minimize invasion by warmwater fish species.
Methods UV and temperature profiling UV and temperature profiles at each of the 11 nearshore sites were taken in June and July 2007, 2008 and 2010, and monthly (except September) from May through October 2009 with a BIC profiling UV-PAR radiometer (Biospherical Instruments, San Diego, CA, USA). The BIC radiometer quantifies incident solar irradiance at
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three different UV wavelengths (305, 320, and 380 nm) as well as visible wavelengths of photosynthetically active radiation (PAR, 400–700 nm) and measures temperature continuously from surface to maximum depth during sampling profiles. Diffuse attenuation coefficients (Kd) were estimated from the slope of the line derived by plotting the log of UV intensity at 305 nm versus depth from BIC profiles. Mean Kd values for June from 2007–2010 were used to calculate UV exposure at 1 m depth as a percent of surface irradiance, except for Sand Harbor and Meeks Bay (2008–2010) and Taylor Creek (2009–2010). UV exposure at 1 m depth as a percent of surface irradiance was calculated by modifying the Beer-Lambert equation that describes the attenuation of light in water, EZ = E0e-KdZ where, E0 is surface UV exposure, Kd is the diffuse attenuation
Fig. 2 Map of Lake Tahoe indicating the location of sample sites. Site numbers correspond with the numbers listed in Table 1
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coefficient derived from BIC profiles, and Z is depth. Nearshore sample sites included: Tahoe Keys East, Crystal Bay, Sand Harbor, Star Harbor, Cave Rock, Emerald Bay and Emerald Bay at Eagle Falls Creek, Sunnyside Marina, Round Hill Pines, Meeks Bay, and Taylor Creek (Fig. 2). Sites were selected to represent the wide range in UV transparency and temperature conditions characteristic of nearshore habitats in Lake Tahoe.
UV exposure experiments: establishing larval UV tolerance For largemouth bass, bluegill, and Lahontan redside larvae, exposure-response relationships of UVinduced mortality were established from outdoor exposure experiments in a temperature controlled environment. Yolk sac larvae were selected for these experiments because their high transparency and lack of mobility are likely to make them the life history stage that is most vulnerable to UV. Here we present methods for largemouth bass and redside minnow experiments, from which the UVAT values were determined. Methods for larval bluegill were similar. Largemouth bass were collected as eggs from a single nest in the Tahoe Keys on June 20, 2009 and hatched in the lab on or before June 23, 2009. On the evening of June 26, 5 yolk-sac larvae were added across treatments to each of 12 treatment dishes (1,750 mL Pyrex crystallizing dishes filled with 1.5 L of 48 lm filtered lake water). Larvae were also added to each of 3 control dishes (1,200 mL plastic bowls filled with 48 lm filtered water). Control dishes were maintained in a temperature controlled environment at 18 °C under low artificial light conditions. Neutral density stainless steel mesh screens (McMaster Carr, Robbinsville, NJ, USA) were placed over the dishes on the morning of June 27 to provide a range of UV exposure levels (100, 78, 57, and 45 % of ambient solar UV). Treatment dishes were then placed in an outdoor water bath and larval survival was monitored every 2 h for 34 h. Dishes were removed from the bath for no longer than 2 min and with the aid of a dissecting microscope, larvae were deemed dead or alive by checking for the heartbeat. Lahontan redside were collected as eggs from Sunnyside Marina on July 15, 2009 and hatched in the lab on July 19 and 20. On the morning of July 22, 10
Development and application of a UV
yolk-sac larvae were added across treatments to each of 12 treatment dishes (250 mL Pyrex crystallizing dishes filled with 250 mL of 48 lm filtered lake water). Larvae were also added to each of 3 control dishes. Control dishes were placed in the water bath with treatment dishes but completely covered in Courtgard (CP Films, Martinsville, VA USA). Courtgard is a long-wave pass plastic that transmits no UVB (295–319 nm; transmits 95 % PAR, 400–800 nm and only 9 % of UV-A 320–400 nm in water with a sharp wavelength cutoff and 50 % transmittance at 400 nm). Neutral density mesh screens were placed over the treatment dishes to provide a range of UV exposure levels (as above for largemouth bass). Treatment dishes were then placed in an outdoor water bath and mortality was recorded every 2 h for approximately 150 h. Mortality was recorded as the cessation of a heartbeat observed under a dissecting microscope. Ambient UV exposure for the duration of these experiments was recorded with a BIC-logging radiometer (Biospherical Instruments, San Diego, California, USA). The radiometer recorded average 305 nm UV intensity (lW cm-2) at 60 s intervals. To calculate 305 nm UV exposure over the course of the experiment the 60 s averages were integrated over time. Because these experiments were conducted on sunny days under predominately cloudless conditions UV exposure was relatively constant. Average 305 nm UV exposure during daylight hours (6:00–20:00) was approximately 3.5 lW cm-2 and varied by less than 8 % among days and tests. A generalized linear mixed effects model was used to determine the effect of UV exposure on the cumulative proportion dead for each larval species. The mixed effects model is a logistic regression model that contains both fixed and random effects (Verbeke and Molenberghs 1997). The fixed effects included species type and exposure level. Because of the random effect of replicate differences the model was fit using PROC GLIMMIX (SAS v. 9.2). The purpose of the ‘0.5/n’ expression in the logit’s numerator and denominator is to insure that predictor settings that result in complete mortality (or complete survival) do not produce an undefined argument for the logit itself. The model accommodates dose/species interaction effects. The indicator variable coding treats redside minnow as a ‘‘baseline’’ species. The model specification was:
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ln
p þ 0:5=n 1 p þ 0:5=n
¼ b0 þ b1 Expo þ b2 IBG þ b3 ILMB þ b4 ðExpo IBG Þ þ b5 ðExpo ILMB Þ þ b0 þ e
where:
pþ0:5=n 1pþ0:5=n
= empirical odds of mortality p =
proportion of sample dead, n = sample size, Expo = cumulative UV exposure, IBG = 1 for bluegill, 0 otherwise, ILMB = 1 for largemouth bass, 0 otherwise, b0 = random intercept effect due to chamber, e = random error. Determining the UV attainment threshold (UVAT) The UVAT was determined as follows: (1)
(2)
(3)
Exposure-response relationships of UV-induced mortality were established from outdoor exposure experiments and used to determine the effective exposure of 305 nm UV to achieve the target amount of bass mortality. Based on a typical approach for determining efficacy of a pesticide (Ritz et al. 2006) we selected a UVexposure level that caused a high amount of mortality (99 %) in bass, but a low amount of mortality in the native redside (\1 %). Cumulative surface 305 nm UV exposure was determined for 4 day periods from a frequency distribution of surface exposure for the month of June 2009, as measured with a ground based GUV- radiometer (Biospherical Instruments, San Diego California, USA). Surface UV exposure was calculated for 4 day windows because 4 days represents a typical, though conservative (i.e. short), incubation period for yolk-sac largemouth bass larvae in the nest before they reach the swim-up stage. The month of June was selected because June represents the peak spawning season for largemouth bass in Lake Tahoe. The UVAT was then calculated simply as the percent of surface 305 nm UV exposure that must penetrate to a given depth (selected by the user, 1 m here) to prevent larval bass survival (i.e. result in mortality of 99 % of the population):
UVAT = 100 (LE99 / E0) where: LE99 = effective UV exposure selected to target bass mortality (kJ m -2) E0 = cumulative 4 day 305 nm UV exposure at surface (kJ m -2)
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In situ incubation experiments: corroborating the UVAT
A. J. Tucker et al. Table 1 UV transparency at each study site as percent of 305 nm UV surface irradiance present at a depth of 1 m Site (*)
Results
% Surface irradiance
Lat
Long
1-Crystal Bay
61
39.24833
-119.98458
2-Sand Harbor
78
39.20680
-119.93213
3-Cave Rock
73
39.04573
-119.94933
4-Round Hill Pines
57
38.98982
-119.95358
5-Tahoe Keys
0
38.89867
-120.00343
6-Taylor Creek
5
38.94043
-120.05770
7-Emerald Bay (EB)
16
38.91505
-120.16820
8-EB- Eagle Falls Creek
2
38.92398
-120.18412
9-Meeks Bay
9
39.03655
-120.12222
10-Sunnyside
61
39.13900
-120.15305
0
39.18260
-120.11892
11-Star Harbor
Percent surface irradiance is derived from mean kd305 values from once monthly June sampling 2007–2010, except sites 2 and 9 (2008–2010 only) and site 6 (2009, 2010 only)
16 14 12
Frequency
In situ incubations were conducted to test the validity of the UVAT. Larval yolk sac largemouth bass used in incubations were collected from a single nest at approximately 1 m depth in the Tahoe Keys. Larvae (n = 5) were placed in Whirl-Pak bags (Nasco, Fort Atkinson, Wisconsin, USA) filled with 100 mL of 48-lm filtered lake water to exclude zooplankton. To isolate the effect of UV between incubation sites, the Whirl-Pak bags were either shielded from incident UV in Courtgard sleeves or exposed to incident UV in Aclar (Honeywell International, Morristown, New Jersey, USA) sleeves. Aclar is a long-wave-pass plastic that in water transmits both PAR (100 % 400–800 nm) and most UV (98 % of UV-B 295–319 nm, 99 % UV-A 320–399 nm, with a sharp wavelength cutoff and 50 % transmittance at 212 nm). Four replicates of each of the UV shielded and unshielded treatments were deployed at one meter depth at a given site for 4 days. After collection, larvae were examined under a dissecting microscope and scored as live if a heartbeat was observed. All procedures involving animals were in accordance with the policies set forth by Miami University’s Institutional Animal Care and Use Committee (IACUC protocol #683).
10 8 6 4 2
UV transparency of nearshore Lake Tahoe varies considerably (Table 1). For the most transparent sites, an average of more than 70 % of 305 nm UV present at the surface penetrated to a depth of 1 m. In the least transparent sites all of the 305 nm UV was attenuated by 1 m. There is also some variability in incident surface exposure due to changes in cloud cover and atmospheric aerosols throughout the month-long study period (Fig. 3). For the month of June 2009, incident surface 305 nm UV exposure for all possible consecutive 4 day periods ranged from 2.7 to 6.2 kJ m-2. The majority of these 4 day windows of time indicated surface exposure somewhere between 4 and 6 kJ m-2. The median surface exposure value of 4.99 kJ m-2 was used to calculate the UVAT. The disparity in UV tolerance of native (Lahontan redside) versus non-native (bluegill and largemouth
123
0 0-1
1-2
2-3
3-4
4-5
5-6
6-7
7-8
305 nm kJ m-2 Fig. 3 Frequency plot of 305 nm UV surface exposure for 4 day windows of time in June 2009 (e.g. of all consecutive 4 day periods in the month of June, 305 nm UV surface exposure was between 3 and 4 kJ m-2 four times). The 4 day window represents a typical (though conservative) incubation period for yolk-sac largemouth bass larvae on the nest before swim-up stage. The median value from this frequency distribution was used in calculating the UVAT (i.e. Eo = 4.99 kJ m-2)
bass) larvae was striking (Fig. 4). The native minnow was more than six times as UV tolerant as largemouth bass and almost 10 times more UV tolerant than bluegill. A UV exposure level of 1.99 kJ m-2 305 nm was lethal to at least 99 % of non-native fish larvae with little or no affect on the native minnows.
Development and application of a UV
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Fig. 4 ‘Exposure-response’ curves from rooftop exposure experiments for bluegill (BG), largemouth bass (LMB) and Lahontan redside minnow (RS) larvae. Dashed lines indicate upper and lower 95 % confidence limits. Calculated LE99 values are displayed (SAS v 9.2 proc GLIMMIX). The LE99 value
(305 nm UV kJ m-2) for largemouth bass was selected as the effective UV exposure level used to achieve the target amount of bass mortality. This UV-exposure level (i.e. 1.99 kJ m-2) induced high mortality (C99 %) in bass and bluegill larvae, but low mortality in the native Lahontan redside larvae (\1 %)
Thus, the UVAT value for the prevention of largemouth bass was estimated to be 40 % (UVAT = 100 [1.99 kJ m-2/ 4.99 kJ m-2]). A total of 5 of 11 sample sites attained the UVAT (i.e.[40 % of surface 305 nm UV exposure was still present at 1 m depth in June, a typical spawning depth and time for largemouth bass in Lake Tahoe), suggesting low probability of successful warmwater fish reproduction. UV transparency did not meet the UVAT standard at the remaining 6 sample sites (Table 2). In situ incubation experiments in UV transparent microcosms support predictions of attainment/ non-attainment (i.e. larval mortality/survival) based on the UVAT (Table 2). Mean survival of larval bass in UV blocking microcosms was C95 % for all sites.
Table 2 Attainment/non-attainment status for 11 nearshore sites based on a UVAT for the prevention of largemouth bass. Sites with greater than 40 % (the UVAT) of surface 305 nm UV exposure still present at 1 m depth are considered in attainment and susceptibility to largemouth bass establishment is reduced. In situ experiments show mean survival (±SE) of largemouth bass larvae in a subset of the sample sites for 4-day incubations at 1 m depth
Discussion Our results demonstrate that the larval stage of a native fish is significantly more UV tolerant than representative non-native warmwater fish larvae. We leveraged this strong species related difference to develop a UV transparency threshold (the UVAT) that could prevent larval warmwater fish survival in Lake Tahoe. In situ incubation experiments across a gradient of UV transparency corroborate the validity of the UVAT
Site
% surface UV @ 1m
Attainment
In situ ± SE
Crystal Bay
61.0
Y
0.0
Sand Harbor
78.0
Y
0.0
Cave Rock
73.0
Y
Round Hill Pines
57.0
Y
Tahoe Keys
0.0
N
Taylor Creek
5.0
N
85.0 (5.0)
16.0 2.0
N N
85.0 (9.6)
Meeks Bay
9.0
N
Sunnyside
61.0
Y
0.0
N
Emerald Bay Emerald @ Eagle Falls Crka
Star Harbor
93.8 (6.3)
a
in non-attainment based on UVAT but not likely susceptible to warmwater fish establishment because of low June temps (see Table 3) 581
(Table 2). Our approach shows that UV transparency of nearshore sites significantly impacts the survival of warmwater fish larvae and may influence whether or
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not these potentially invasive fish species are able to establish throughout nearshore Lake Tahoe. By quantifying the effect of UV exposure on the earliest life history stage of warmwater fish and measuring levels of this important abiotic factor in nearshore Lake Tahoe our research provides critical new insights that will allow managers to more cost effectively control and prevent warmwater fish invasion. In particular this approach allows lake managers to identify ‘at risk’ sites where systematic monitoring and early detection efforts for non-indigenous species can be targeted. In this example ‘at risk’ sites represent locations in the nearshore environment where warmer water temperatures and reduced UV transparency provide a refuge for reproduction of warmwater fish. From our analysis, ‘at risk’ sites are those sites where, for the month of June, water temperature is greater than the lower limit for bass spawning and less than 40 % of surface 305 nm UV is present at a depth of 1 m. Our analysis was based on observations that suggested June spawning at 1 m depth is typical for largemouth bass in Lake Tahoe. We used a very conservative lower thermal limit of 12.7 °C for bass spawning (Wallus and Simon 2008). Water temperature at 1 m depth in June exceeded 12.7 °C for 9 of 11 sample sites (Table 3). In calculating the UVAT of 40 % we assumed normal UV conditions (i.e. median June 305 nm surface exposure, see Fig. 3). Based on these criteria six of the eleven study sites are ‘at risk’ of bass establishment, assuming the presence of reproductive adults. Emerald Bay at Eagle Falls Creek was in non-attainment based on UV exposure but low water temperature in June likely precludes successful bass spawning at this site. Regular monitoring of these ‘at risk’ sites increases the likelihood of early detection and the potential for successful implementation of control measures. This approach also increases cost effectiveness of management efforts because: (1) it focuses efforts in space (i.e. on ‘at risk’ sites) and (2) focuses management efforts in time, by assessing the possibility of larval survival based on temperature and UV during the warmwater fish spawning season. Effective monitoring programs are still likely to require substantial effort to succeed in stemming the spread of invasive species. For example, a successful monitoring program for the presence of warmwater fish nests in Lake Tahoe would at the very least include plans to survey ‘at risk’ sites during the months of possible warmwater fish spawning and at depths where
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nest establishment is most likely. Our nearshore survey data suggest that in most years water temperature in Lake Tahoe is suitable for spawning in ‘at risk’ sites beginning in June. In some sites (e.g. Tahoe Keys) water temperature exceeds 12.7 °C beginning in May (Table 3). Therefore, a comprehensive monitoring program for Lake Tahoe needs to consider site specific temperature data and initiate at least biweekly surveys to ensure nest detection. Furthermore, even though we have not observed bass spawning after early July in Lake Tahoe, water temperatures are still suitable for spawning well into summer, and even into early fall in some locations (Table 3), which might warrant continued monitoring later into the growing season. On the other hand, largemouth bass are not known to have especially protracted spawning seasons (Wallus and Simon 2008) and age-0 bass survival is known to depend largely on size at overwintering while recruitment to age 1 favors fish spawned earlier in the season (Miranda and Hubbard 1994; Ludsin and DeVries 1997; Garvey et al. 1998). Also, despite observations suggesting that the majority of largemouth bass spawning occurs at less than 1 meter in Lake Tahoe (an observation consistent with descriptions from the literature that report typical nest depths of 15 cm to 2 m, Carlander 1977), the most thorough monitoring program may require surveys up to 10 meters in depth. Nevertheless, the identification of ‘at risk’ sites based on the UVAT significantly reduces
Table 3 Temperature (°C) at 1 m depth (or maximum depth if less than 1 m) for all sample sites from BIC profiles. Sampling dates were from 2009 as follows: May 12–13, June 18–20, July 16–18, Aug 27–29, Oct 1–2 Site
May
June
July
Aug
Oct
Crystal Bay
9.5
15.3
17.3
19.8
16.6
Sand Harbor
9.6
13.7
16.6
19.2
17.2
Cave Rock
13.9
16.2
18.1
16.3
Round Hill Pines
14.5
18.1
18.0
15.7
15.8
18.3
21.2
19.4
14.9
10.0
19.1 14.9
22.2 18.4
16.4 18.6
11.2 16.2
11.5
16.8
14.5
17.2
16.7
10.3
12.5
15.6
18.5
15.8
12.8
15.5
17.4
6.7
Tahoe Keys Taylor Creek Emerald Bay (EB) EB- Eagle Falls
14.9
Creek Meeks Bay Sunnyside Star Harbor
7.9
Development and application of a UV
the workload for managing invasions by identifying target sites and constraining monitoring times. Coupling the UVAT approach with other more traditional metrics could even further constrain monitoring efforts and costs. For example, in lakes where managers already have data on other metrics for bass success (e.g. substrate availability, food resources, and adult presence or absence), ‘priority at risk’ sites could be identified that, based on multiple metrics (including UV), are most likely to support reproduction of invasive warmwater species. At its best this approach might eliminate monitoring costs altogether, as sustained high levels of UV throughout a lake could effectively prevent invasion. Thus managing water clarity to maximize underwater UV levels may be an important end goal in itself. Dissolved organic carbon (DOC) is often the most important regulator of UV transparency in aquatic systems (Morris et al. 1995; Rae et al. 2001) and has been called the ‘ozone of the underwater world’ (Williamson and Rose 2010). DOC may be especially important in nearshore habitats where fish spawning occurs, since DOC inputs are likely to be concentrated in those areas. For example, in Lake Tahoe, chromophoric dissolved organic matter absorption coefficients for stream water were 10 times higher than offshore values (Swift 2004). Water quality analysis of nearshore sites in Tahoe shows that UV transparency in the nearshore is strongly dependent on DOC concentration though the best model for predicting UV transparency included both DOC and chlorophyll (Tucker et al. 2010). The influence of inorganic particulates on UV transparency has not been assessed in Lake Tahoe. Efforts to quantify the relative importance of each of these factors in controlling UV transparency (especially in ‘at risk’ sites) and adapting management approaches accordingly could prove to be an effective approach for preventing the establishment of aquatic invaders. For example, whether or not best management practices (BMPs) and other water clarity improvement measures move sites toward UV attainment thresholds could be an additional criterion for evaluating the effectiveness of BMPs. In Lake Tahoe, BMPs and water clarity improvements have focused largely on reducing levels of organic and inorganic particulate matter (Schuster and Grismer 2004). Where these efforts are effective in improving water clarity they are also likely increasing underwater UV exposure and therefore
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moving sites toward a UVAT standard that could prevent warmwater fish invasion. However, given the important role that DOC plays in regulating UV transparency in nearshore Lake Tahoe management practices that are tailored to increase underwater UV levels in particular (e.g. by reducing [DOC]) may be a more cost-effective means of both increasing water clarity and preventing warmwater fish spread. Although few lakes are as highly transparent as Lake Tahoe, estimates from DOC measurements in North American lakes indicate that UVR transparency is relatively high throughout western, northwestern, and southeastern portions of the USA (Williamson et al. 1996). This suggests that the UVAT could have broad geographic relevance. For example, based on modeling the relationship between DOC concentration and UVR attenuation, the depth to which 1 % of 320 nm UV surface irradiance penetrates is greater than 1 m in 75 % of lakes sampled in the western United States. About 25 % of these lakes exhibit 1 % 320 nm UV depths greater than 4.75 m. In the Alps and Pyrenees of Europe a survey of 26 lakes found 1 % UVA depth ranges of 1.1 to 46.1 meters (Laurion et al. 2000). The DOC concentration in most of the transparent lakes sampled in the North American study is quite low (i.e. \1 mg/L) and mean DOC concentrations in the European study were 0.97 mg/L, suggesting that even small changes in DOC could significantly reduce current UVR levels in these lakes (Williamson et al. 1996). There are important caveats to consider in the development and application of the UVAT. For instance, DOC concentrations and water clarity in lakes are strongly dependent on rainfall (Pace and Cole 2002). Although climate data from the National Climatic Data Center show that the long term trend in summer precipitation (1895 to present) for the Tahoe region remains flat (http://www.ncdc.noaa.gov), heavy rainfall events are generally increasing around the globe (Karl et al. 2009). Prolonged cloudy periods or persistent nearshore plumes high in DOC could expand refugia for invasive warmwater fish and might require generally higher water transparency for the UVAT to be effective. Similarly, stochasticity in ‘average’ surface irradiance could also affect the utility of the UVAT. The UVAT that we report here was based on median surface irradiance for June 2009. Although long-term UV surface irradiance data for the Tahoe region are not currently available, hourly
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observations of sky cover from the National Climatic Data Center for the period 2001–2011 indicate that June 2009 was cloudier than the ‘average’ June. In fact, sky cover in June 2009 was more than 20 % higher than the mean for that period, suggesting that lower water transparency than predicted by our UVAT might successfully stem warmwater fish invasion in Tahoe’s nearshore environment. Ideally UV irradiance data will become more broadly available in the future and subsequent efforts to develop water clarity thresholds will be able to incorporate longer term averages of UV surface irradiance. Furthermore, whereas we have emphasized the implications of declining water clarity for biological invasion there may be some equally interesting implications for invasion in aquatic habitats that experience increases in transparency. For example, submersed macrophytes are generally most abundant and species rich in clear-water lakes (Scheffer et al. 1993; Toivonen and Huttunen 1995), although oligotrophic clear-water lakes (the trophic state characteristic of most cold, clear, alpine systems) tend to support fewer macrophytes than mesotrophic or eutrophic lakes (Rorslett 1991). Nevertheless, light decays exponentially under macrophyte canopies (Westlake 1964). Hence, an increase in the abundance of submersed vegetation that might occur after an increase in water transparency could potentially provide refuge for the establishment of UV sensitive species in otherwise clear-water systems. On the other hand, macrophyte stands also generally reduce water temperature, by as much as 10 °C m-1 in one study (Dale and Gillespie 1977), which could decrease habitat suitability for certain temperature sensitive invaders. Interestingly, increased water transparency has been documented as a consequence of reduced turbidity following the introduction of invasive Dreissena (Skubinna et al. 1995), suggesting that invasive species themselves could potentially mediate biological invasion through their impacts on water clarity. These more complex interactive effects of biological invaders, water transparency, and temperature need to be explored. Meanwhile, in the context of UVAT management, more ‘complex’ habitat types (like macrophyte beds) could be treated as ‘at risk’ sites and regularly monitored for the presence of invasive species. We have suggested that UV can be an important factor in controlling aquatic invasive species establishment in
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transparent lakes. The development of UV attainment thresholds could therefore be an important tool to manage and prevent biological invasion in numerous aquatic systems. Our method is not unlike the threshold approach that others have used to develop maps of invasion risk (Neary and Leach 1992, Whittier et al. 2008; for zebra mussels), except that we have identified a novel factor (UV exposure as a function of water transparency) that is relevant for at least warmwater fish establishment in more transparent lakes. The extent to which this novel indicator can be applied to other aquatic invaders should be carefully explored. We contend that this approach will have relevance for any UV sensitive species that is constrained to shallow water environments in more transparent lakes. It may, for example, be a useful tool for the management of invasive bivalves, which are generally restricted to littoral and sublittoral zones, often require relatively warm water temperatures for reproduction, and at least in some cases appear to be sensitive to UV exposure (Gilroy 2003). Regardless of the specific geographic or taxonomic context in which it is employed the UVAT will increase the cost effectiveness of aquatic invasive species control by focusing management efforts in space (on ‘at risk’ sites) and time (during spawning season), and it will allow managers to evaluate the effectiveness of BMPs in terms of their ability to prevent biological invasion by selecting water clarity improvement methods that most effectively increase underwater UV transparency. In this ‘era of globalization’ the magnitude of the biological invasion threat only continues to grow (Hulme 2009). The UVAT is one more tool that may enhance our ability to predict and prevent species invasion in aquatic systems. Acknowledgments We thank Geoff Schladow and the staff of the Tahoe Environmental Research Center for their assistance. Sudeep Chandra and Christine Ngai (University of Nevada-Reno), Mark Olson (Franklin and Marshall College), and Tom Crist (Miami University) provided helpful input on this manuscript. Neil Winn created the GIS map of Lake Tahoe. John Bailer and Michael Hughes of the Statistical Consulting Center of Miami University provided data analysis assistance. Michael Cohen, Ian Lizzadro-McPherson, Amanda Gevertz, Annie Bowling, Jeremy Mack, Kevin Rose, and Sandra Connelly provided field assistance. The experimental design for in situ incubations was borrowed from Mark Olson. This work was supported in part by funding from Miami University’s Field Workshop Program, USDA Forest Service, Pacific Southwest Research Station, Southern Nevada Public Land Management Act #8-3D01, NSF DEB-IRCEB0552283, and NSF DGE-0903560.
Development and application of a UV
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