Special Issue: ETAE (Emerging Trends in Aquatic Ecology) III
Light pollution enhances temporal variability of
photosynthetic activity in mature and developing biofilm
Maggi E.*, Bertocci. I., Benedetti-Cecchi L.
Dipartimento di Biologia, CoNISMa, Università di Pisa, via Derna 1, I-56126, Pisa (Italy)
*corresponding author: elena.maggi@unipi.it 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19
Abstract
Artificial light at night (ALAN) has been recently recognized as a threat for aquatic systems, but a comprehensive knowledge of its effects is still lacking. A fundamental question is whether and how ALAN might affect temporal variability of communities, thus undermining the stability of mature assemblages or influencing the colonization process. Here we investigated the role of ALAN on temporal variability of total biomass and maximum photosynthetic efficiency of marine autotrophic biofilms colonizing Mediterranean high-shore rock surfaces, while controlling for density of their main grazers. Results showed stability in total biomass, but an increase in maximum photosynthetic efficiency from unlit to lit conditions, which suggested a temporal change in composition and/or abundance of different taxa within mature assemblages. The effect was weaker during the
colonization process; in this case, density of grazers acted in the opposite direction of ALAN. We suggest that the addition of light at times when it would not be naturally present may affect the temporal variability of a variety of functioning in aquatic systems, depending on species-specific sensitivities to ALAN within microbial assemblages and/or indirect effects mediated by their consumers. We highlight to further investigate the role of this emergent topic in aquatic ecology.
Keywords: artificial light at night, temporal variability, marine microbiomes, autotrophs
Introduction
The high rate of human growth is causing a dramatic increase in urbanization at a global scale (Seto et al., 2012), which in turn is related to a variety of disturbances for terrestrial and aquatic organisms. This represents a pressing problem especially for systems such as shores, lakes, riverine zones and estuaries, where human presence is mostly concentrated (Yang & Bowling, 2014; Neumann et al., 2015; Van Niekerk et al., 2019). The presence of artificial light at night (ALAN) is something we are so used, that scientists have recognized it as a key source of pollution very recently compared to other less visible threats related to urbanization. Indeed, by modifying 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
natural light/dark alternation, ALAN may act on a plethora of physiological and ecological
processes involving both autotrophic and heterotrophic organisms, including humans (Gaston et al., 2013; Gaston, 2018). Only in the last few years scientific attention has been turned on biological effects of ALAN in aquatic systems, giving first insights on potential influences on physiology and behavior of microbes, invertebrates and vertebrates (e.g., Davies et al., 2015; Hölker et al., 2015; Navarro-Barranco & Hughes, 2015; Bolton et al., 2017; Manfrin et al., 2018).
Aquatic microbiomes play a critical role in biochemical cycles and in many life stages of macro-organisms, as cues for settlement of spores and larvae, food for herbivores, as well as within the holobiont concept (e.g. Underwood, 1979; Thompson et al., 2000; Sanz-Lázaro et al., 2015; O’Connor & Richardson, 1998; Huang & Hadfield, 2003; Egan et al., 2013; Longford et al., 2019). In addition, marine surface associations of micro-organisms (or biofilms) have been recently recognized as a source of large microbial diversity with still unknown functional potentials (Zhang et al., 2019).
Research on effects of ALAN on aquatic microbiomes has revealed that it may affect both primary producers and heterotrophic organisms (Grubisic et al., 2018; Maggi & Benedetti-Cecchi, 2018), and even induce a transformation of inland waters to nocturnal carbon sinks in freshwater systems (Hölker et al., 2015). Moreover, the specific nature and magnitude of effects may drastically depend on the intensity and type of the light source. This confirms the key role of the spectral region of emission and light levels of artificial lamps in relation to species-specific sensitivity thresholds (Davies & Smyth, 2017). This is of particular concern considering that outdoor lightings worldwide are being replaced by high intensity white LEDs, which, although energetically efficient, are rich in blue wavelengths, within the visible spectrum some of the most impacting for terrestrial and aquatic organisms (Gaston, 2018).
Despite some recent advances, however, our understanding of potential effects of ALAN on biofilms, and aquatic organisms in general, is still at the beginning and there is an urgent need for studies deepening critical physiological and ecological aspects. These include the fundamental 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 66 67 68 69 70 71
question of whether and how ALAN would affect the temporal variability of target response variables. Changes in temporal variability of community variables, such as total abundance, productivity or other functional responses may be the result of different biological mechanisms, such as synchronous, asynchronous or compensatory responses of singular taxa to the same or different factors (Micheli et al., 1999, and references therein). The study of temporal variability of assemblages under changing abiotic and biotic conditions is therefore the first step to identify the most plausible processes involved in the stability of ecosystems. Moreover, it is reported that changes in patterns of fluctuations may indicate a system that is approaching a critical threshold before a potentially catastrophic ecological shift (Wissel, 1984; van Nes & Scheffer, 2007; Scheffer et al., 2012). Finally, the study of changes in temporal variability is a priority within the topic of ecological successions, characterized by temporal patterns of species occurrence and replacement after a disturbance event (Connell & Slatyer, 1977; Tilman, 1990). Very different temporal
fluctuations of response variables may occur even provided their comparable values averaged over time (e.g., Bertocci et al., 2005).
Here, we investigated the potential role of ALAN on temporal variability of total biomass and maximum photosynthetic efficiency of marine autotrophic biofilms (microphytobenthos, hereafter MPB), colonizing Mediterranean high-shore rock surfaces, usually above the sea level and wetted by waves only during sea storms. The MPB is a fundamental component of assemblages at this height on natural and artificial rocky shores, being the main food resource for invertebrates and main primary producers (Thompson et al., 2000). The ubiquitous occurrence of MPB assemblages at the interface between air and water makes them directly exposed to effects of ALAN, caused by the presence of coastal streets and promenades, as well as harbors, ports and marinas. Moreover, MPB is composed by taxa with short generation times, which further contributes to make it an excellent system to investigate the potential effects of light pollution on the temporal variability of relevant response variables.
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Light pollution is expected to directly influence MPB by making light available at night for the photosynthetic process and by altering species fitness (Jacquet et al., 2001; Raven & Cockell, 2006; Poulin et al., 2016). It is reasonable to suppose, however, that singular (groups of) species composing MPB assemblages have different sensitivities to light intensity and spectra (Davies & Smyth, 2017). Consequently, temporal changes in maximum photosynthetic efficiency and biomass under lit conditions might be species-specific, with potential alterations to the temporal variability of corresponding aggregate variables (Micheli et al., 1999). In addition, grazers might be able to reduce temporal variability of their resource (MPB) through continued biomass consumption (mean-variance relationship; Taylor, 1961). If ALAN affects the activity or density of grazers, its effects might cascade on MPB temporal variability and interact with direct effects of ALAN, as recently observed for values of MPB biomass shortly after the recolonization process (Maggi & Benedetti-Cecchi, 2018). We therefore tested for possible effects of ALAN on temporal variability of responses at whole MPB assemblage level (namely, on total photosynthetic biomass and
maximum photosynthetic efficiency), while controlling for effects of grazers. To check for possible effects of the mean-variance relationship, we also tested for the same effects on mean temporal values of biomass and maximum efficiency.
Materials and methods
The study was carried out on a rocky coast in the Western Mediterranean Sea, within a limited access location owned by the Italian Navy (Maralunga, La Spezia, Italy; 43°28’02 N, 10°22’19 E). The geographical area is characterized by a narrow tidal range. High on the shore (0.2 - 0.4 m above Mean Low Water Level) assemblages are dominated by epilithic biofilms, whose main component is represented by MPB, mostly cyanobacteria; Maggi & Benedetti-Cecchi, 2018; Maggi et al., submitted). Main grazers are littorinid snails [namely, Melaraphe neritoides
(Linnaeus, 1758)], which are more active under moist conditions, such as during sea storms or rain 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121
events (Dal Bello et al., 2017; Maggi et al., 2017). Other grazers are virtually absent in the high shore.
Experimental design and collection of data
In March 2016, we selected four sites 5-10 m long and 30-40 m apart. Values of night sky brightness measured at these sites indicated the presence of a relatively dark sky (mean ± SE: 20.14 ± 0.02 mag/arcsec2, measured through a Unihedron Sky Quality Meter-L, during new moon phase). Intensity of light at night in absence of the moon was virtually null (0.00 lux, measured through a luxmeter, RS PRO model ILM 1332A). Sites were evenly and randomly allocated to the lit treatment or to control conditions (lit and unlit sites, respectively). At each lit site, ALAN was simulated with a cold white LED lamp (Labcraft, 12.5W), mounted on a vertical stainless-steel pole secured to the rock high on the shore. White LED lamps are characterized by a light spectrum that includes all the visible wavelengths, with a main peak in the blue region (e.g., Davies & Smyth, 2018). Light was automatically switched on at dusk and off at dawn. Distance among lit and dark sites was enough to ensure that artificial lighting did not influence unlit sites. At each site, we randomly selected six quadrats of 10x10 cm (tens cm apart), with similar distance and orientation with respect to the lamp (intensity of artificial light at lit sites: mean ± SE = 27.33 ± 4.01 lux): three were left untouched (control), while access of snails was prevented in the remaining three quadrats (exclusion) by applying an organic glue along the entire perimeter (Tree Tanglefoot, pesticides free). Frequent visits to the study sites confirmed that snails were almost absent from exclusion quadrats; the few rarely present were immediately removed. Previous studies indicated the lack of effects on MPB due to the presence of the glue (Dal Bello et al., 2017; Maggi & Benedetti-Cecchi, 2018). After 3, 22, 45 and 64 days since the start of experimental manipulations, we counted the number of snails within each quadrat and estimated the photosynthetic biomass and the maximum photosynthetic efficiency of MPB by means of a Diving PAM (WALZ). Previous studies conducted in the same system showed that this temporal scale was appropriate for investigating temporal variation within MPB assemblages (Sanz-Lazaro et al., 2015; Dal Bello et al., 2017). For each 122 123 124 125 126 127 128 129 130 131 132 133 134 135 136 137 138 139 140 141 142 143 144 145 146 147
replicate quadrat at each sampling date, data were obtained by averaging two values of minimum fluorescence (F0) and two values of quantum yield of Photosystem II (Yield = (Fm- F0)/Fm;
Fm=maximum fluorescence; dark adaptation period of 5’; Maggi et al., 2015), obtained by taking
two measurements within each quadrat. Measurements were conducted in the morning.
In November 2016, we repeated the experiment to assess potential effects during the process of recolonization by MPB. In this case, the eight randomly selected quadrats (10x10cm) at each site were scraped clean with a chisel mounted on a battery drill, to initiate succession (Maggi &
Benedetti-Cecchi, 2018). The experiment run for a longer period compared to the previous one, to let the MPB assemblage develop. The same measurements described above were conducted after 25 (no biofilms had developed earlier), 104, 151 and 204 days after the start of the experiment. For both experiments, dates of sampling were randomly chosen as representative of the experimental period (Fig. S2 and Fig. S3).
Data analyses
Firstly, for both experiments, we calculated the values of mean temporal density of snails for each replicate quadrat. Values were analyzed by means of a three-way ANOVA, with Herbivore (two levels: control, exclusion) and Light (two levels: lit and dark) as crossed fixed factors, and Site (two levels) as a random factor, nested within Light and crossed with Herbivore. Homogeneity of variances was checked through Cochran’s test (gad and C.test functions within GAD package, R project). Analyses showed a significant variability among sites in the first experiment, while no effect of ALAN (Table S1 and S2; Figure S1). To take into account the potential spatial variability in the effect of grazers, we opted for including the mean temporal density of snails (calculated for each replicate quadrat) as a covariate in the analyses on temporal variability of aggregate
community variables, instead of including the potential source of variability related to the
presence/absence of herbivores as a fixed, categorical factor. For consistency, we applied the same analytical tool to both experiments.
148 149 150 151 152 153 154 155 156 157 158 159 160 161 162 163 164 165 166 167 168 169 170 171 172
To estimate the temporal variability of aggregate community variables, data on photosynthetic biomass (F0) and maximum photosynthetic efficiency (Yield) of total MPB
assemblage from each sampling date were used to calculate the temporal variance in F0 and Yield for each replicate quadrat, for both runs of the experiment. Temporally very variable patterns of an estimated variable would be quantified by relatively large values of its variance calculated over the period of the study, while a null variance would be ideally shown by a variable that occurred to be fully constant over time. Data were also used to calculate mean temporal values of the same variables. Due to the presence of both fixed and random categorical factors (Light and Site nested within Light, respectively) and a covariate (mean density of snails), data were analyzed by means of mixed-effect models, with Light and mean density of snails in the fixed part of the model and Site and replicate quadrats in the random one (lmer function within lme4 package, R project).
Results
Mature MPB assemblage
Analyses showed no significant effects of either the factor ALAN or the covariate mean density of grazers on temporal variance of photosynthetic biomass, but a significant increase in temporal variance of maximum photosynthetic efficiency under ALAN conditions (Table 1, Figure 1).
Analyses on mean temporal values of F0 and Yield showed a significant increase in maximum photosynthetic efficiency of mature MPB assemblages at increasing density of grazers (Table 2).
Developing MPB assemblage
Analyses showed no significant effects of either the factor ALAN or the covariate mean density of grazers on temporal variance of photosynthetic biomass, but a marginal increase in maximum photosynthetic efficiency of developing MPB under ALAN conditions (0.05<p<0.1), 173 174 175 176 177 178 179 180 181 182 183 184 185 186 187 188 189 190 191 192 193 194 195 196 197
after accounting for a significant decrease of Yield at increasing density of grazers (Table 1, Figure 1).
Analyses on mean temporal values of F0 and Yield showed a significant increase both in biomass and maximum photosynthetic efficiency under ALAN conditions, after accounting for a decrease at increasing density of grazers (only marginal for F0; 0.05<p<0.1) (Table 2).
Discussion
Light pollution at night is a global phenomenon, tightly related to urbanization, that
represents a potential source of disturbance for many aquatic systems (Davies et. al., 2015; Hölker et al., 2015; Falchi et al., 2016; Gaston, 2018). Within these, assemblages living at the interface between air and water are those more directly exposed to terrestrial sources of artificial light. Our results showed that white LED lamps mimicking coastal urban lightings at night can increase the temporal variability in maximum photosynthetic efficiency of MPB colonizing rocky habitats high on the shore, with effects on both the mature assemblage and during the colonization process.
Understanding the responses of populations and assemblages to anthropogenic changes is a key challenge in ecology and the investigation of temporal variability in assemblages represents a useful tool to predict the stability of ecosystems under changing abiotic and biotic conditions (Donohue et al., 2016; Radchuk et al., 2019). The increase in temporal variance of a response variable is expected to be positively related to disturbance (Micheli et al., 1999) and has been revealed as an early warning signal of approaching regime shifts in perturbed aquatic ecosystems (Carpenter et al., 2011). The increase in temporal variability of community response variables under disturbed conditions may be driven by different biological processes. For MPB assemblages
exposed to ALAN, it is possible that singular (groups of) species undergo either synchronous or asynchronous larger temporal fluctuations in the variable of interest (Micheli et al., 1999), in comparison to unlit conditions, because of frequent physiological adjustments to light pollution. Increased temporal variance may also imply a greater probability of extinction (Inchausti & Halley, 198 199 200 201 202 203 204 205 206 207 208 209 210 211 212 213 214 215 216 217 218 219 220 221 222 223
2003) and therefore be indicative of temporal changes in species composition. Finally, within assemblages composed by organisms with short generation times such as MPB, an increase in temporal variance may be related to changes in species relative abundances (Bertocci et al., 2005, 2017; Oliveira et al., 2014).
Here, we observed variable effects of light pollution on temporal variability of MPB, depending on the response variable, the stage of development of the assemblage and the mean density of grazers. MPB biomass showed no changes in its temporal variability from unlit to lit conditions at night, neither in mature or developing assemblages, nor related to mean density of grazers. Previous studies on effects of ALAN on aquatic micro-organisms revealed idiosyncratic effects on abundance and activity of primary producers, depending on the intensity and type of the lighting source (high pressure sodium or LED), as well as on the time of exposure and the identity of organisms. Among cyanobacteria, the freshwater Microcystis aeruginosa (Kützing) Kützing was negatively affected by even short pulses of low levels of high-pressure sodium lighting (HSD, 6.6. lux), which decreased its photosynthetic activity, but not growth, under laboratory conditions (Poulin et al., 2016). On the contrary, abundance of phototrophic bacteria in freshwater sediments was positively affected by long-term in situ exposure (1 year) to similar intensities and type of light, and their photosynthetic activity was stimulated at night by white LEDs at high intensity (71 lux) (Hölker et al., 2015). The same LED lamps, but at a moderate intensity (20 lux), caused a
significant decrease in periphyton abundance of sub-alpine streams (which included cyanobacteria; Grubisic, 2017, 2018). Data from the present study revealed no effects of white LED lighting at intermediate intensity (about 27 lux) neither on temporal variability nor on mean photosynthetic biomass in mature cyanobacterial assemblages (the largely dominant fraction of MPB at the study site; Maggi et al., submitted). Interestingly, temporal stability in biomass (shown by a lack of significant effects on temporal variance of F0) from unlit to lit conditions was associated with an increase in temporal variability of maximum photosynthetic efficiency, independently of the grazing pressure (i.e. mean density of littorinid snails). This result may be explained by an increase 224 225 226 227 228 229 230 231 232 233 234 235 236 237 238 239 240 241 242 243 244 245 246 247 248 249
in temporal fluctuations of maximum photosynthetic efficiency of invariant taxa composing mature MPB, and by temporal changes in composition and/or relative abundances of organisms
characterized by diverse photosynthetic efficiencies (such as different cyanobacterial species, diatoms or macroalgal spores), due to a selection through time for taxa more adapted to conditions generated by ALAN. Although both explanations are plausible and not mutually exclusive, if the first mechanism was the dominant one, we would also expect an effect on temporal fluctuations in MPB biomass, but this was not observed. In addition, unpublished data from meta-barcoding analyses at the end of the experiment highlighted a significant increase in diversity indices of cyanobacterial assemblages under lit conditions (Maggi et al., submitted), which in part
corroborates the second scenario. Although the system maintained a stable biomass through time, the significant increase in temporal variability of maximum efficiency may imply the impairment of other functions related to the composition and relative abundances of MPB taxa, such as rates of nitrogen fixation (Carpenter et al., 1991).
Similar mechanisms may be responsible for the marginal increase (0.05<p<0.1) in temporal variability of maximum photosynthetic efficiency from unlit to ALAN conditions in developing assemblages. In this case, it is worth noting that the effect on the variance might be, at least in part, due to an increase in mean temporal values of the same variable, consistently with the mean-variance scaling relationship (Taylor, 1961). Classical theories of ecological successions predict temporal changes in composition and abundance of organisms during the process of colonization of bare substrate, mediated by competitive or facilitative interactions among early and late colonizers (e.g., Connell & Slatyer, 1977; Farrell, 1991). Our results suggest that exposure to LED lighting at night may enhance temporal changes in composition and /or relative abundances of taxa composing MPB assemblage, likely fostering ecological succession through facilitative mechanisms. In
addition, this positive effect could have been mediated by the increase in mean temporal MPB biomass under lit conditions. Similarly to what has been observed in intertidal macroalgal 250 251 252 253 254 255 256 257 258 259 260 261 262 263 264 265 266 267 268 269 270 271 272 273 274
assemblages, increases in abundance of early colonizers can interact with their identity and richness in driving different successional patterns in MPB assemblages (Maggi et al., 2011).
Contrarily to what was observed for MPB mature assemblages, mean density of grazers negatively affected temporal variability in maximum photosynthetic efficiency during the colonization process, although a direct grazers density-dependent mechanism for this outcome is difficult to envision. Negative effects of density of grazers on mean temporal biomass and mean maximum photosynthetic efficiency, however, suggest that grazers could have reduced the mean relative biomass of selected components of MPB assemblages, such as those photosynthetically more efficient. Eventually, low biomass of relatively less efficient MPB components would have necessarily reduced the temporal variability of MPB maximum efficiency (mean-variance
relationship).
The lack of a negative effect of grazers on mature MPB assemblages can be ascribed to several mechanisms. Consumption rates of littorinid snails could not be high enough to overwhelm a positive effect on MPB due to removal of dead cells (Skov et al., 2010; Maggi et al., submitted), or to counteract the productivity rates of abundant species composing mature MPB. Alternatively, the assemblage may be composed of low palatability taxa. Selective feeding of littorinid snails on specific MPB taxa seems to be corroborated by, once again, their negative effect on mean temporal maximum photosynthetic efficiency.
While we recognize the speculative nature of most of the processes and mechanisms hypothesized as plausible explanations of our findings, and we admit that environmental factors other than light (e.g., temperature and humidity) may also play a combined and potentially
interactive role, with this study we suggest a plethora of pathways through which ALAN can affect MPB assemblages and microbial biofilm in general, ultimately aiming at stimulating further
research on an emergent topic. Our results, in particular, suggest that the addition of light at times when it would not be naturally present may differentially affect singular components of
photoautotrophic microbial biofilm, due to species-specific sensitivity and/or indirect effects 275 276 277 278 279 280 281 282 283 284 285 286 287 288 289 290 291 292 293 294 295 296 297 298 299 300
mediated by temporally variable effects of their consumers. For example, littorinid snails are more active during cold months (Dal Bello et al., 2015; Maggi et al., 2017), which could explain the negative effect of ALAN documented on them only during the colonization experiment. Further research and specifically designed experiments are needed to clarify the mechanisms potentially able to drive stability in MPB assemblages in different aquatic habitats exposed to light pollution. These should include, for example, intertidal estuarine systems and tidal flats, where MPB play a critical role for primary productivity, sediment stability and as food resource for several
invertebrates, fish and shorebirds (Serôdio & Catarino, 2000; Tolhurst et al., 2003; Como et al., 2014). In particular, assemblages dominated by diatoms are subject to daily vertical migrations within the photic zone, in response to tidal and day/night cycles (Serodio et al., 2001; Consalvey et al., 2004), as well as to ‘micro-migrations’ within the surface layers, where specific taxon
sequentially move up and down to escape photoinhibition (Underwood et al., 2005).
Future studies will increase our ability to predict the effects of ALAN in aquatic systems, and to understand their possible interactions with other disturbances already impinging on these and other systems threatened by current and future human activities (Davies and Smyth 2018).
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Table 1. Results of mixed-effects models (MEM) for temporal variance of photosynthetic biomass (F0) and maximum photosynthetic efficiency (Yield) of MPB. For fixed effects, estimates with standard errors (within brackets) are shown. Significance of probability associated with fixed effects is shown as follows: §0.05<p<0.1, *p<0.05. For random effects, estimates of variance associated with Sites and replicates are given.
Temporal variance
Fixed effects Mature MPB Developing MPB
F0 Yield F0 Yield
Light 996.6 (13892.3) 4·10-3 (1.4·10-3)* 1641.5 (2240.7) 7.7·10-4 (3.4·10-4)§ Density of snails 130.5 (1070.2) 7.7·10-5(1.1·10-4) -740.0 (593.2) -1.8·10-4 (7.9·10-5)* Random effects
Site 2.095e-06 0.000 0.000 2.448e-08
Replicate 1.102e+09 1.145e-05 2.576e+07 4.560e-07
Table 2. Results of mixed-effects models (MEM) for temporal mean of photosynthetic biomass (F0) and maximum photosynthetic efficiency (Yield) of MPB. Significance of probability associated with fixed effects is shown as follows: §0.05<p<0.1, *p<0.05. For random effects, estimates of variance associated with Sites and replicates are given.
323 324 325 326 327 328 329 330 331 332 333 334 335 336 337 338 339
Temporal mean
Fixed effects Mature MPB Developing MPB
F0 Yield F0 Yield
Light -30.62 (65.35) 0.026 (0.008) 47.28 (17.73 )* 0.012 (0.005)* Density of snails 2.223 (2.380) 5·10-4 (6·10-4)** -9.44 8( 4.69 ) § -0.003 (0.001)* Random effects
Site 3459 0.000 0.000 0.000
Replicate 4593 3.566e-04 1612 1.124e-4
Legend to figure
Figure 1. Mean temporal variability (+1SE) of photosynthetic biomass (F0) and maximum photosynthetic efficiency (Yield; F0 and Yield values taken after a dark adaptation period of 5’) under experimentally lit and unlit conditions, in mature and developing MPB assemblages. Values indicate the partial residuals of temporal variance in F0 and Yield after accounting for mean density of grazers and random effects associated to different sites in mixed effect models. Note differences in scale. 340 341 342 343 344 345 346 347 348 349 350 351 352 353 354 355
Mature MPB assemblage
Photosynthetic biomass Maximum photosynthetic efficiency 356 357 358 359 360 361 362 363 364 365 366 367
Developing MPB assemblage
Photosynthetic biomass Maximum photosynthetic efficiency
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