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Phyc_34_502.772_778

J. Phycol. 34, 772–778 (1998)
EXPERIMENTAL MESOCOSM STUDIES OF SALINITY EFFECTS ON THE BENTHIC ALGAL Sierra Nevada Aquatic Research Laboratory, University of California, Route 1, Box 198, Mammoth Lakes, California 93546 Department of Biological Sciences, Northern Arizona University, Flagstaff, Arizona 86001 As closed-basin systems, saline lakes are prone to fluc- Mono Lake; periphyton; salinity; salt lakes tuate in level and salinity with climate change and hydro-logic alterations. Loss of many Great Basin lakes has re- Inland saline lakes within closed hydrologic basins sulted from the diversion of tributary streams for agricul- are subject to natural and induced fluctuations in tural or municipal uses. At Mono Lake, an alkaline salt size and salt concentration over both short and long lake in eastern California, salinities have risen from 50 to time intervals. Global and regional climate changes 100 g·LϪ1 in just 50 years. Experimental mesocosms were have altered Holocene lake chemistry in North established to simulate some of the potential ecological ef- America, as evidenced both in paleohydrological fects that could have accompanied this change. The influ- data (e.g. Benson and Thompson 1987, Stine 1990) ence of salinity on diatom diversity, taxonomic structure, and in paleobiological indicators such as the diatom and primary production was tested using mesocosms de- stratigraphy of sediments (e.g. Bradbury 1987, Fritz ployed at Mono Lake. Mesocosm tanks were 500 L in vol- 1990, Blinn et al. 1994). More recent changes and ume, 1 m square, and 0.5 m deep, with open tops covered drying of Great Basin lakes have resulted from the by 1 mm mesh net. Five treatments (50, 75, 100, 125, diversion of tributary streams for agricultural or mu- and 150 g·LϪ1) with four replicates per treatment were used nicipal uses. At Mono Lake, an alkaline salt lake in over a 2-month period. The diatom-dominated benthic al- eastern California, approximately half the volume of gae were reduced both in standing crop (from 6 to Ͻ0.1 the lake was lost in the 50 years following stream g·mϪ2) and diversity (from 30 to 12 taxa) with increased diversions that began in 1941. Lake levels have risen salinity, with most loss occurring in salinities Ն75 g·LϪ1. recently following wet years and an order by the Cal- Photosynthetic oxygen production also was significantly ifornia State Water Resources Control Board to re- lower at salinities Ն75 g·LϪ1. Diatom indicator taxa for turn stream flow to the lake. Management and pro- these shifts included Denticula sp., Nitzschia frustulum, tection of these changing ecosystems depend upon N. monoensis, N. communis, and Stephanodiscus an understanding of the influence of salinity on bi- oregonicus increasing in relative abundance in higher ological productivity and community structure. The salinity treatments, accompanied by decreases in Achnan- goal of our research was to predict ecological thes minutissima, Cymbella minuta, N. dissipata, and changes along temporal salinity gradients associated Rhoicosphenia abbreviata. Exhibiting dominance at with rising and falling lake levels. The present paper moderate salinity levels (75 to 125 g·LϪ1) were Nitzschia describes benthic algal dynamics with emphasis on frustulum, N. communis, N. palea, and Navicula cru- the distribution of diatom diversity.
cialis. These latter species may be limited by both physio- Previous studies of salt lake benthic algae have logical stress at high salinity and grazing and competition focused on distributions in surveys of lakes with both at low salinity. The filamentous chlorophyte, Ctenocladus varied salinities and environmental settings (Ham- circinnatus, and cyanobacteria (Oscillatoria spp.) oc- mer et al. 1983, Blinn 1993, 1995), or laboratory curred only in salinity treatments from 50 to 100 g·LϪ1. cultures of isolated species over a salinity range Diversion of tributary stream flow and resulting salinity (Blinn 1984, Herbst and Castenholz 1994). Studies increases in this lake threaten sustained benthic primary of mixed species cultures of algal mat from saline production and algal species diversity relative to conditions lakes showed growth yields were reduced by salinity prior to stream diversion. The 1994 decision of the Cali- but did not examine changes in species composition fornia State Water Resources Control Board to return (Herbst and Bradley 1989). Though the traditional stream flows to Mono Lake will raise the lake level and use of laboratory bioassays has yielded much infor- reduce salinity to around 75 g·LϪ1 and is expected to in- mation on physiological chemical toxicity, there are crease the diversity and productivity of the benthic algae of limited data integrating the response of aquatic communities to salinity stress. Experimental micro-ecosystems or microcosms provide a valuable ap- 1 Received 31 December 1997. Accepted 6 May 1998.
proach for more realistic simulations integrating the 2 Author for reprint requests; e-mail herbst@lifesci.ucsb.edu.
community level response to ecological variables (Kimball and Levin 1985, Cooper and Barmuta1993). Though freshwater lake research has utilizedmicrocosms, few studies of saline lake ecosystemshave used this method to examine benthic com-munities, even though shallow-water habitats are anideal application. Here, we use the term ‘‘meso-cosm’’ to distinguish the size and duration of ex-perimental salinity treatments employed in theseMono Lake studies (Cooper and Barmuta 1993). Ex-perimental field mesocosms permit more authenticsimulations of salinity effects on the benthic littoralecosystem of Mono Lake because mesocosms allowenvironmental control, replication, and manipula-tion of salinity in understanding how this variablemay regulate a mixed community of algae and in-vertebrates. These mesocosms are also appropriatecomparisons to the shallow-water environment (Ͻ1m deep) where most production occurs (Herbst andBradley 1993). Results may be used to approximatehistorical and future ecological changes and to aidin the design of lake restoration plans to optimizeecological values (productivity and diversity). Thisresearch will find further application in the inter-pretation of paleoenvironmental climate changebased on diatom stratigraphic records from lake sed-iment cores and in understanding the dynamics ofsaline lake food chains.
The effects of salinity on the structure and productivity of the benthic algal community of Mono Lake were tested in large fi-berglass mesocosm tanks (1- by 1-m sides, 0.5 m deep, open topscovered with 1 mm mesh net) located in a shallow concrete basinabout 100 m from the shore of Mono Lake, California. Water was Latin square array of mesocosm tanks at Mono Lake, pumped from Mono Lake through a 200-␮m mesh screen into California. No salinity treatments were repeated in rows or col- 20 tanks to a depth of 45 cm (near 500 L). Salinities were grad- umns. Photovoltaic panels were used to charge deep cycle batter- ually adjusted in each mesocosm over a 5-week period by dilution ies, which powered the aeration system.
with water from nearby Lee Vining Creek and/or by replacementof evaporated water with hypersaline Mono Lake water to thedesired target salinity levels of 50, 75, 100, 125, and 150 g·LϪ1.
(Mono Lake salinity was ca. 100 g·LϪ1 at the time of these exper- treatment level was monitored with submerged maximum-mini- iments in 1991.) Each salinity level was replicated four times, and tank treatments were arrayed in a Latin square design (Fig. 1).
Algal production was estimated by measuring dissolved oxygen During the 5-week acclimation period, 10 L of sand substrate concentrations in each mesocosm over a full day-night period, from Mono Lake were added to each tank, followed by 2 L of using the light:dark periods to estimate net photosynthesis and mixed fine organic sediments. Upon reaching the target salinities, respiration, respectively. Dawn, dusk, noon, and midnight read- each mesocosm was further inoculated with 5 L of Mono Lake ings were taken with a YSI model 58 oxygen meter equipped with sediments containing algal mats and associated invertebrates. In a model 5739 probe. Net daytime oxygen production was added addition, to serve as external colonization sources from a wide to night respiration to determine gross photosynthetic oxygen salinity range, 0.5 L of sediments from nearby Black Lake (salinity production. Standing crop of periphyton at the end of the ex- ca. 50 g·LϪ1) and 0.5 L of sediment from hypersaline Mono Lake periment was determined by measuring chlorophyll a according onshore ponds (ca. 150 g·LϪ1) were added to each mesocosm to Lind (1979) from scrubs of algae attached to the outside of tank. Evaporated water from each mesocosm was replaced every submerged air-lift tubes of known area. These suspended tubes 3–5 days over the course of the experiment with water from Lee were isolated from grazing by benthic ephydrid larvae, but were Vining Creek, holding salinities to within less than 10% deviation colonized by the same type and amount of diatoms and filamen- from target levels. Aeration was supplied from a single high vol- tous algae found on benthic substrates in each treatment. This ume air pump (43 L·minϪ1 capacity) with air lines to plexiglass provided a standard measure for comparing periphyton density air-lift tubes in each tank, and was powered by photovoltaic panels over all treatments that was independent of grazing.
charging a deep-cycle battery system (Fig. 1). The air pump op- Taxonomic composition of benthic diatoms was determined erated through a remote timer on daily cycles of 16 h on and 8 from benthic surface sediment cores (12.6 cm2) at the end of the h off. This aeration, along with daily temperatures that typically 2-month experiment. Samples were oxidized by the hydrogen per- ranged between 15Њ and 25Њ C in all tanks and treatments, pro- oxide-dichromate method (van der Werff 1955). Slides were pre- vided water circulation and oxygenation. Water samples for nu- pared in Hyrax௡ mounting medium, and diatom taxa were count- trient ammonium analysis were taken after mesocosm filling and ed at magnifications of 1400ϫ. A minimum of 300 valves was at the initiation and termination of the experiment (indophenol counted for each experimental replicate (i.e. mesocosm), and the blue method; Strickland and Parsons 1972). Temperature of each average relative abundance of each diatom taxon (based on cell Mean percent relative abundance (ϮSE), number of taxa, and Shannon diversity of diatom communities in sediments from Mono Lake mesocosm experiments for selected salinity treatments after 8 weeks of incubation. Achnanthes minutissima Ku¨tz.
Amphora pediculus (Ku¨tz.) Grun.
Anomoeoneis sphaerophora (Ehr.) Pfitz.
Cymbella minuta Hilse ex. Rabh.
Fragiliaria construens v. venter (Ehr.) Grun.
Fragilaria fasiculata (Ag.) Ku¨tz.
Fragilaria vaucheria (Ku¨tz.) Peters.
Gomphonema subclavatum (Grun.) Grun.
Navicula crucialis (O. Mu¨ll.) Frenguelli Navicula cryptocephala Ku¨tz.
Navicula cryptonella Lange-Bertalot Nitzschia dissipata (Ku¨tz.) Grun.
Nitzschia monoensis Kociolet et Herbst Nitzschia palea (Ku¨tz.) W. Sm.
Nitzschia reimerii Kociolek et Herbst Rhoicosphenia abbreviata (Ag.) Lange-Bertalot Stephanodiscus oregonicus (Ehr.) Hak.
counts) was determined for each salinity treatment. Diatom cells munity of Mono Lake mesocosms occurred for a sa- were unlikely to have appeared in sample counts of cleaned frus- linity change from 50 to 75 g·LϪ1, with only minor tules unless some survival and growth of cells occurred. Differ-ential growth and survival under varied salinity conditions pro- changes in biotic indices in treatments Ͼ75 g·LϪ1 duced consistent patterns of diatom distribution in each treat- (Table 1). The Shannon diversity index dropped ment rather than the random sampling of rare cells across treat- from 4.0 to 2.6 and the number of diatom taxa de- ments that would be expected if dead cells or empty frustules creased from 30 to 15 between treatments of 50 and were an important component of benthic samples.
Samples for algal periphyton other than diatoms were taken 75 g·LϪ1. Blinn (1993) also reported a strong neg- from the south-facing walls of each tank after 2 months using a ative relationship between salinity and HЈ diversity razor blade to scrape 20-cm2 areas. When feasible, a minimum of and richness of diatom taxa in saline lakes of west- 40 cell dimensions were taken from each treatment replicate for ern North America, with the greatest decline in bi- the primary forms found, filaments of Ctenocladus circinnatus Borzi(Chlorophyceae) and cyanobacteria (mainly Oscillatoria spp.). Es- otic indices at salinities Ͼ45 mS specific conduc- timates of biovolume (␮m3·cmϪ2) for C. circinnatus and cyanobac- tance (near 50 g·LϪ1). Blinn (1995) found a similar teria were made for each salinity using a Palmer counting cham- relationship in diatom communities of the saline ber at 400ϫ. Calculations of biovolume were based on the volume lakes of Western Victoria, Australia. Furthermore, Statistical comparisons of the effects of salinity treatments were Wilson et al. (1996) reported Ͻ20% of the 204 di- made using one-way ANOVA. Chlorophyll a biomass data were atom taxa used in assessing salinity inference models log transformed prior to analysis, and multiple comparisons were had an upper tolerance limit of Ն50 g·LϪ1 salinity.
made using Scheffe’s test. A diversity index (HЈ) was calculated Denticula sp., Nitzschia frustulum, N. monoensis, N. for diatom assemblages for each treatment (Shannon and Weaver1949).
communis, and Stephanodiscus oregonicus increased inrelative importance in higher salinity treatments, making up over 70% of the diatom assemblage at The greatest change in species richness and di- 125 to 150 g·LϪ1 (Table 1). In contrast, Achnanthes versity of the diatom-dominated benthic algal com- minutissima, Cymbella minuta, N. dissipata, and Rhoi- Mean cell widths and lengths (m; Ϯ SE) and biovolumes (m cmϪ2; ϮSE) for Ctenocladus circinnatus and filamentous cyanobacteria from various mesocosm salinity treatments after 8 weeks of incubation. cosphenia abbreviata decreased in relative importance the dominant diatom taxa in nonmarine saline en- in elevated salinities. Although Wilson et al. (1996) vironments, whereas N. dissipata and R. abbreviata reported that S. oregonicus was tolerant only of mod- have only a moderate tolerance to elevated salinities.
erately high salinities (upper limit of 19.4 g·LϪ1), The clearly salt-tolerant N. monoensis was recently de- our study showed this species tolerant of salinities scribed by Kociolek and Herbst (1992) from deep up to 150 g·LϪ1. Nitzschia frustulum, N. communis, N. sediments in Mono Lake and has also been found palea, and Navicula crucialis exhibited dominance at in Owens Lake cores (Bradbury 1993). These and intermediate salinity levels (75 to 125 g·LϪ1). These other taxa exhibiting clear trends in the studies re- taxa are among the most common species in salt ported here may be useful as indicator signals for lakes of western North America, and our results are calibrating paleolimnological studies. Reconstruc- consistent with the intermediate salinity hypothesis tion of ancient lake levels using diatom stratigraphy (Herbst 1988), which suggests the abundance of has been based on correlations with distributions these halophiles may be controlled by ecological fac- along environmental salinity gradients (e.g. the tors, such as grazing and competition, at low salinity, transfer functions of Fritz et al. 1991). Mesocosm and by physiological intolerance at higher salinities.
results may permit a more direct and accurate cali- Ephydrid larvae were most productive in low salinity bration of stratigraphic records against the actual mesocosms; thus, it is possible that increased grazing growth response of mixed species assemblages of di- activity may also have contributed in part to the atoms and other benthic algae exposed to changing higher diatom diversity observed at 50 g·LϪ1 salinity through cropping of competitive dominants (grazer- The dramatic decrease in species richness at salin- ities Ͼ50 g·LϪ1 further suggests that evolutionary Other studies have shown similar patterns in dia- pathways for the radiation of lacustrine diatom spe- tom community structure with elevated salinities.
cies occurred along salinity gradients that ranged Blinn (1993) and Wilson et al. (1996) reported that from sea to freshwater rather than from seawater to certain species of Denticula as well as Nitzschia frus- hypersaline conditions. Blinn (1993) further sup- tulum tolerate relatively high salinities and are often ports this hypothesis in a study of 63 North Ameri-can saline lakes, where he shows a striking increasein the number of diatom taxa at specific conduc-tance loadings Ͻ45 mS, with the greatest species di-versity in waters dominated by NaCl rather than incarbonate or sulfate waters. This may indicate thathighly saline nonmarine habitats provided only lim-ited opportunity for the radiation of marine diatomsduring the Oligocene and that these habitats pre-sented physiological barriers to colonization. Theimportance of saline lake environments in the adap-tive radiation of diatoms into lacustrine ecosystemsrequires laboratory studies in molecular genetics tofurther develop this hypothesis.
The filamentous chlorophyte, Ctenocladus circin- natus, occurred in salinity treatments ranging from50 to 100 g·LϪ1. Over this growth range, there was Standing crop of periphyton in Mono Lake meso- a significant (F ϭ 5.2, P ϭ 0.01) decrease in the cosms, expressed as log-transformed chlorophyll a taken fromsamples of tank air-lift tubes. Error bars indicate standard devia- biovolume density of this alga at higher salinities tions for four replicates per salinity treatment level.
(Table 2). Average biovolumes were Ͼ40-fold high- below 100 g·LϪ1 (Herbst 1988, Herbst and Casten-holz 1994).
In addition to lower total biovolume, Ctenocladus cell width increased and length decreased with ele-vated salinity (Table 2). Width of cells averaged 5.6and 9.7 ␮m, and length 118.1 and 53.7 ␮m, in treat-ments of 50 and 100 g·LϪ1, respectively. Blinn andStein (1970) and Blinn (1971) also found that celldimensions of C. circinnatus became wider andshorter or formed akinetes under increased salini-ties. Herbst and Castenholz (1994) noted similarchanges in cell size in C. circinnatus at salinities Ͼ50g·LϪ1 and suggested that a lower surface-to-volume Mesocosm metabolism expressed as net photosynthetic ratio may reduce osmotic water loss from cells ex- oxygen production during daylight hours (lower cross-hatched posed to high external salt concentrations.
portion of bars) and oxygen consumption by respiration during The average biovolumes of cyanobacteria in the the night (upper open portion of bars); total bar height estimatesgross photosynthetic oxygen production. Diel measurements of various salinity treatments were several orders of dissolved oxygen changes taken 1 month into the 2-month ex- magnitude lower than those for C. circinnatus (Table periment. Error bars indicate standard deviations for four repli- 2). Cyanobacteria also were absent from salinity treatments Ͼ100 g·LϪ1 and were variable at lowersalinities, but they showed no significant differences er at 50 than at 100 g·LϪ1, and cells were not ob- (P Ͼ 0.1) as noted in C. circinnatus. The absence of served above 100 g·LϪ1. These findings agree with these Oscillatoria spp., capable of nonheterocystous those of Ruinen (1933), Blinn (1971), and Herbst nitrogen fixation, from high salinity treatments sug- and Castenholz (1994), where threshold salinity for gests that nitrogen fixation by cyanobacteria may be akinete germination and vegetative growth was be- confined to lower salinity levels. Nitrogenase activity tween 100 and 150 g·LϪ1. This salt-tolerant alga has in Mono Lake sediments has also been found to be been reported from a number of saline lakes inhibited by salinity (Herbst, unpubl.).
throughout North America (Blinn and Stein 1970, There were significant reductions in chlorophyll Blinn 1971, Hammer et al. 1983, Hammer 1986) a of benthic algae (F ϭ 9.4, P ϭ 0.001) and meso- and is a common constituent of the phytobenthos cosm net photosynthesis (F ϭ 10.7, P ϭ 0.001) be- in Mono Lake and Abert Lake (Oregon) at salinities tween salinity treatments (Figs. 2, 3). A post hoc Ammonium nutrient levels in experimental mesocosm salinity treatments. Samples taken during salinity acclimation phase, at experiment initiation (inoculation), and at termination (2 months after initiation). Error bars indicate standard deviations for fourreplicates per salinity treatment level.
Scheffe multiple comparison test on log-trans- to permit the best conditions for production and formed data of chlorophyll a standing crops showed diversification of benthic algae in Mono Lake. Pro- significant differences (alpha ϭ 0.05) as follows: 50 longed salinity exposures above 100 g·LϪ1 without Ͼ 75 Ͼ 100 Ͼ 125 ϭ 150 g·LϪ1. Mesocosm metab- local low salinity refugia on lake and playa margins, olism, however, showed differences only between 50 could limit the capacity of Mono and other saline g·LϪ1 and all other treatments. The large decrease lakes to support large populations of consumers.
in periphyton chlorophyll a standing crop without aconcomitant drop in net photosynthetic oxygen pro- duction may have resulted from chlorophyll a esti- Mono Lake is one of a few perennial deep alka- mates having been made on attached algae, whereas line salt lakes in the world (Melack 1983). Diversion net oxygen production of mesocosms was the prod- of tributary stream flow and resulting salinity in- uct of both planktonic and benthic photosynthesis.
creases in this lake threaten sustained benthic pri- It is possible that planktonic algae increased in the mary production and algal species diversity relative higher salinity treatments and maintained oxygen to conditions prior to stream diversion. Evidence of production even while benthic algae were reduced.
such changes was shown in experimental meso- This is supported by the observation that turbidity cosms where the prediversion salinity of 50 g·LϪ1 was sometimes higher in tanks at high salinity treat- supported significantly higher periphyton chloro- ments, possibly due to the presence of halophilic phyll a biomass and twice the diatom diversity found phytoplankton such as Dunaliella, which has opti- at higher salinity treatment levels. Lower salinities mum growth above 100 g·LϪ1 (Javor 1989).
supported greater biomass and diversity of algae de- The nitrogen source in Mono Lake occurs mainly spite the availability of more ammonium in the high- in the form of ammonium (Jellison et al. 1993). Am- er salinities. Maintenance of a benthic algal com- monium in mesocosm tanks was found to increase munity is critical to aquatic foodwebs in saline eco- with salinity before inoculation (ranging from about systems, because these primary producers are the 5 to 20 ␮M, Fig. 4) but was depleted in all treat- principal food source of brine flies of the genus ments at termination of the experiment. This sug- Ephydra, often the dominant benthic invertebrate of gests that while all treatments supported biological saline lakes in the Great Basin. These invertebrates uptake activity, benthic primary production was re- in turn support diverse and abundant bird com- duced at high salinity even though more nitrogen munities that frequent these habitats. The 1994 de- was available. Greater nutrient availability apparent- cision of the California State Water Resources Con- ly cannot compensate for the inhibitory effects of trol Board ordering the return of stream flows to Mono Lake was based in part on the evidence of Although caution should be used in applying the lost production and diversity presented in this pa- results of mesocosm experiments to nature (Carpen- per. The Water Board order will raise the lake level ter 1996), separate laboratory and field observations and reduce salinity to around 75 g·LϪ1 and is ex- support the conclusions and generality of our stud- pected to enhance the diversity and productivity of ies. Independent data from field surveys (Blinn the benthic algae of this ecosystem.
1993) and lab cultures (Herbst and Castenholz1994) are consistent with our interpretation of salin- Benson, L. V. & Thompson, R. S. 1987. Lake level variation in ity constraints on periphyton production and diver- the Lahontan Basin for the past 50,000 years. Quat. Res. 28:69–85.
Blinn, D. W. 1971. Autecology of a filamentous alga, Ctenocladus This work contributes to an understanding of sa- circinnatus (Chlorophyceae), in saline environments. Can. J. line lake food chains because diatoms and other benthic algae form the primary food source of the 1984. Growth responses to variations in temperature and specific conductance by Chaetoceros muelleri (Bacillariophy- alkali fly Ephydra (Hydropyrus) hians Say (Diptera: ceae). Br. Phycol. J. 19:31–5.
Ephydridae), often the dominant benthic inverte- 1993. Diatom community structure along physicochemi- brate of many alkaline salt lakes and ponds in the cal gradients in saline lakes. Ecology 74:1246–63.
Great Basin (Herbst 1988, Bradley and Herbst 1995. Diatom community structure along salinity gradi- 1994). This insect and other Ephydra species are in- ents in Australian saline lakes: biogeographic comparisonswith other continents. In Kociolek, P. & Sullivan, M. [Eds.] tegral to saline lakes as wildlife habitats because they A Century of Diatom Research in North America. Special Sympo- support the food requirements of dozens of species sium for Reimer and Patrick Festschrift. Koeltz Scientific of shorebirds and waterfowl, which may number in Books, Champaign, Illinois, pp. 163–74.
the hundreds of thousands (Boula 1985, Jehl 1994, Blinn, D. W., Hevly, R. H. & Davis, O. K. 1994. Continuous Ho- locene record of diatom stratigraphy, paleohydrology, and Rubega and Inouye 1994, Elphick and Rubega anthropogenic activity in a spring-mound in Southwestern 1995). Few of these productive lakes remain in the United States. Quat. Res. 42:197–205.
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Printed in Germany · All rights reserved _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ Teaching Cataloguing and Classification at the University of Pretoria: Thinking Preferences of Second Year Students ANN-LOUISE DE BOER, H. S. COETZEE, H. COETZEEDepartment of Information Science, University of Pretoria, Queenswood, South AfricaThe information profession has c

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