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A Comparison of the oxygenating differences of invasive non-native Lagarosiphon major and native Ceratophyllum demersum

A Comparison of the oxygenating differences of invasive non-native Lagarosiphon major and native... Downloaded from https://academic.oup.com/biohorizons/article/doi/10.1093/biohorizons/hzy008/5151366 by DeepDyve user on 10 August 2022 BioscienceHorizons Volume 11 2018 10.1093/biohorizons/hzy008 ............................................................................................ ..................................................................... Research article A Comparison of the oxygenating differences of invasive non-native Lagarosiphon major and native Ceratophyllum demersum Rhiann Mitchell-Holland , Nicola Jane Morris and Peter Kenneth McGregor Centre for Applied Zoology, Cornwall College Newquay, Newquay TR7 2LZ, UK *Corresponding Author: Rhiann Mitchell-Holland. Email: rhiann01@hotmail.com Supervisor: Peter McGregor ............................................................................................ ..................................................................... Native to Southern Africa, Lagarosiphon major is a submerged macrophyte that is recognized as a problematic, invasive non-native species in many countries including the UK. It is widely sold and promoted through the aquarium and water gar- den industry as an ‘efficient oxygenator’ for freshwater systems, irrespective of the absence of evidence to support this statement and evidence of its adverse ecological and economic impacts. A key concern, relating to its rapid growth rate and high fresh weight density, is that L. major can impose self-shading and limitation of photosynthetic and respiratory activity, causing it to consume more oxygen than it produces. Low dissolved oxygen (DO) conditions typify diminished water quality and seriously limit oxygen-dependent organisms. We measured over several months the DO, fresh weight and associated pond life abundances of L. major and a comparable UK-native macrophyte, Ceratophyllum demersum, estab- lished in small-pond conditions to determine which species best maintained a healthy freshwater environment. Both the time from establishment and species had significant effects on DO concentrations and pond life abundance; L. major pro- duced the least amount of oxygen over time and had significantly less associated pond life compared to the native plant. L. major also increased significantly in overall fresh weight compared to C. demersum, indicating the higher invasive ability of the non-native species. In conclusion, our results suggest that L. major is not as good an oxygenator as C. demersum and that this native species should be promoted through the aquarium and water garden trades as an efficient oxygenator that improves water quality and habitat conditions over time. Key words: invasive non-native species, macrophytes, dissolved oxygen, pond life, fresh weight, water quality Submitted on 24 October 2017; editorial decision on 10 September 2018 ............................................................................................ ..................................................................... Strayer et al., 2003; Dudgeon et al., 2006; Riis et al., 2012). Introduction In cases where such plants have outcompeted and replaced As a result of worldwide travel and trade, numerous invasive native submerged vegetation (Rattray, Howard-Williams, species have been introduced, both intentionally and inadvert- Brown, 1994; Keenan, Baars, Caffrey, 2009), severe depletion ently, into areas beyond their natural range (Westphal et al., of dissolved oxygen (DO) and diminished water quality has 2008; Stiers, Njambuya, Triest, 2011). Aquatic plant species been the result (Caraco et al., 2006; Leppi, Arp, Whitman, invasion has been recognized as one of the largest threats to 2016). Organisms, such as freshwater fish, invertebrates, freshwater ecosystems and biodiversity, with detrimental con- plants and bacteria, rely on DO (the level of free, non- sequences for ecology and the economy (Pimentel et al., 2000; compound oxygen present in water) for survival, thus cannot ............................................................................................... .................................................................. © The Author(s) 2018. Published by Oxford University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. Downloaded from https://academic.oup.com/biohorizons/article/doi/10.1093/biohorizons/hzy008/5151366 by DeepDyve user on 10 August 2022 Research article Bioscience Horizons � Volume 11 2018 ............................................................................................... .................................................................. withstand anoxic (a total depletion of oxygen) or even hyp- pH values that create further complications for many aquatic oxic (low oxygen) conditions for extended periods of time vertebrate and invertebrate species (Sand-Jensen, 1989; (Gray, Wu, Or, 2002; Caraco et al., 2006; Lenntech, 2015). Hussner et al., 2014). Due to the decidedly invasive nature of The presence and abundance of organisms and organic mat- L. major, which has already been banned in New Zealand ter (and their associated biological processes) can greatly and Australia (Natural Heritage Trust, 2003), it is an offence influence DO concentrations in a body of water (Caraco to plant or otherwise allow this species to grow in the wild in et al., 2006; Desmet et al., 2011; Kemker, 2013; Ribaudo, the UK, under Schedule 9 of the Wildlife and Countryside Bertrin, Dutartre, 2014). For example, while photosynthesis Act (NNSS, 2016). However, natural checks on the growth contributes to an increase in DO (Desmet et al., 2011), the of L. major in the UK are insufficient, and control/eradica- process of respiration by organisms, and decomposition of tion of the species is extremely costly and often ineffective organic matter by microorganisms, can severely deplete the (Caffrey, 1993; Caffrey and Monahan, 2006; Stiers, available DO for aerobic species (Caraco et al., 2006; Njambuya, Triest, 2011; European Parliament, 2014). Desmet et al., 2011; EPA, 2012; Annis, 2014). Despite high Despite its environmental, ecological and economic DO productivity during the day (Carrillo, Guarín, Guillot, impacts, L. major is a popular water garden/aquarium plant, 2006; Ribaudo, Bertrin, Dutartre, 2014), dense clusters of often sold as Egeria or Elodea densa through the aquatics aquatic plants can cause water hypoxia at night, particularly industry (NNSS, 2011; J. Newman, personal communica- in slow-moving water bodies, as the rate of oxygen con- tion). The UK population of L. major has been intentionally sumption at the lower level of the bed cannot be replenished planted as an ‘oxygenator’ and is often promoted through the by diffusion from the atmosphere (Mazzeo et al., 2003; trade as one of the best (Natural Heritage Trust, 2003; Nault Loverde-Oliveira et al., 2009). Quantifying the impact of and Mikulyuk, 2009; CBD, 2011; CABI, 2016; Royal abundant macrophytes on basic water quality (oxygen Horticultural Society, 2016). Its English common name ‘oxy- dynamics, nitrogen retention and nutrient concentrations), gen weed’—referring to the species’ ability to add oxygen to Desmet et al. (2011) found that diurnal and seasonal fluctua- the water as a result of its high photosynthetic rate (Rattray, tions of DO were strongly correlated with plant growth/bio- Howard-Williams, Brown, 1994; CABI, 2016)—is the likely mass density, temperature and solar irradiance, observing reason behind the industry’s promotion of the plant. water hypoxia during the summer. Since light and tempera- However, the high biomass densities that are characteristic of ture are triggers for biological processes, these diurnal and this macrophyte are likely to lead to a higher consumption seasonal shifts can be affected by climatological conditions; than production of oxygen, seriously limiting other aquatic such findings match literature knowledge about the impacts of species (Natural Heritage Trust, 2003; Nault and Mikulyuk, dominating macrophytes on DO dynamics (Natural Heritage 2009). The trade of this plant as an ornamental through the Trust, 2003; Tadesse, Green, Puhakka, 2004; Hussner, Internet and mail order greatly increases its obtainability and Hofstra, Jahns, 2011; Riis et al.,2012). ease of spread to new locations (Kay and Hoyle, 2001; An invasive non-native species of particular concern is Australia Natural Heritage Trust, 2003; CABI, 2016). Lagarosiphon major (Ridley) Moss. L (Hydrocharitaceae). Much of the existing literature regarding L. major focuses Native to South Africa, this submerged macrophyte is a con- on the core factors affecting aquatic plant growth and siderable potential threat to static water bodies in many morphology, such as temperature/light conditions (Desmet countries, including the UK, where it is now well established et al., 2011; Riis et al., 2012), availability of carbon and (Bowmer, Jacobs, Sainty, 1995; NNSS, 2011; J. Newman, nutrients (Hussner et al., 2014)orcompetitive abilities personal communication). In addition to the aforementioned (Stiers, Njambuya, Triest, 2011; Martin and Coetzee, 2014). problems associated with aquatic plant species invasion, L. However, little attention has been paid primarily to the oxy- major has been observed forming dense canopies that often genating abilities of L. major, with seemingly no existing lit- occupy entire water volumes of slow-moving water bodies erature that directly measures its effects on DO over time. (Stiers, Njambuya, Triest, 2011). These thick mats block Thus, in addition to filling this gap in the literature, our light penetration to other flora (eliminating their growth), study aimed to compare L. major as an oxygenator with the restrict water movement and interfere with recreation activ- UK-native macrophyte, Ceratophyllum demersum (rigid ities, ultimately exacerbating flood risks (Schwarz and hornwort). C. demersum was chosen based on its similar Howard-Williams, 1993; McGregor and Gourlay, 2002; morphological and growth characteristics to L. major. Stiers, Njambuya, Triest, 2011). Ceratophyllum demersum is also widely sold as an oxygen- As with other aquatic invasive species, L. major outcom- ating plant and is recognized as invasive outside of its nat- petes native aquatic vegetation and affects associated popula- ural range, although it does not share as many of the tions of species as it has a rapid growth rate and is effectively inherent risks as L. major (McGregor and Gourlay, 2002). perennial, surviving through the winter (Keenan, Baars, Our experiment also measured and compared the differences Caffrey, 2009; NNSS, 2011; J. Newman, personal communi- in growth (fresh weight) and associated pond life abundance cation). Furthermore, it is effective at removing CO and and diversity of the two species over 12 weeks to assess their HCO − from water via photosynthesis, resulting in very high invasiveness and habitat impact. ............................................................................................... .................................................................. 2 Downloaded from https://academic.oup.com/biohorizons/article/doi/10.1093/biohorizons/hzy008/5151366 by DeepDyve user on 10 August 2022 Bioscience Horizons � Volume 11 2018 Research article ............................................................................................... .................................................................. mesh coverings were considered to exclude organisms and Materials and Methods organic matter. However, in order to retain natural light irradiance and temperature of the water, and in turn Plant sample collection strengthen the integrity of the experiment (since contamin- Healthy plant samples of C. demersum (800 g) and L. major ation is a natural occurrence in ponds), the buckets were (800 g) were collected from two adjacent ponds (A6 and A8) instead, monitored daily for major debris contamination at Penrose Water Gardens, Truro Cornwall (Fig. 1)on 7 (floating leaves, dead insects, etc.); anything found was October 2015. As pond A8 was larger than pond A6, samples removed with a sieve promptly. were only collected within an area of similar size to pond A6 (boundary indicated by dotted line, Fig. 1), ensuring that both Parameters measured species derived from similar depth, light, temperature and Six weeks after establishment, DO (mg/L) and temperature growth conditions to limit the degree of variation in morph- (°C) of the water in each bucket were measured twice a week ology. Samples were collected with a rake and by hand from for 12 weeks (10 December 2015–3 March 2016) using randomly selected areas of the two ponds, avoiding sample Hanna Instruments (Leighton Buzzard, UK) HI9142 portable selection bias and retaining sample independence. All samples waterproof DO meter and a TPI-315C (Crawley, UK) digital were rinsed thoroughly on site (within ponds), and again later thermometer. Data collection always began at 1 h and 20 min with settled tap water, to ensure no invertebrates or other after sunrise to control for diurnal effects on DO (informed plant species were present; any found were returned to their by pilot study, personal observation) and collected in a respective ponds, or a nearby garden pond at the study site. balanced order to limit the degree of variation between buck- ets over time. The DO meter was left for 15 min before any Experimental setup measurements were taken to allow time for equilibration (fol- The experiment was conducted outdoors in Truro, Cornwall, lowing manufacturer’s recommendations), and a 1-min per between October 2015 and March 2016. Simulating small- bucket time limit was allocated for DO and temperature read- pond conditions, 200 g of L. major and 200 g of C. demersum ings. Along with DO and temperature parameters, the date, of similar size and root length were placed into plastic buckets hours since sunrise, general weather conditions (by visual containing 8 L of settled tap water. Tap water was left to inspection) and water volumes of each bucket were also stand for over 48 h prior to plant introduction (following recorded. Water levels were controlled every other day and Stiers, Njambuya, Triest, 2011) and had a mean (±S.E.) DO kept at ~8000 cm per bucket. If a significant amount of water of 9.6 (±0.049) mg/L; thus simulated pond conditions were was lost or gained as a result of condensation or rainfall (i.e. similar at the start of the experiment. In total, 12 buckets— ±>5cm of original volume), it was replaced with settled tap four replicates of each species and four containing only water water, or removed in order to keep conditions the same, and as controls—were left to establish for 6 weeks (from 29 reduced the potential of algal growth or algae bloom through October 2015 to 10 December 2016) before any measure- water replenishment (Paerl et al., 2001; Stiers, Njambuya, ments were taken. All buckets were situated on a raised Triest, 2011). Buckets were rearranged every other day, decked area ~0.5 m above ground level. As highlighted by again, in a balanced order, to reduce the effects of variation many researchers (Caraco et al., 2006; Desmet et al., 2011; of light and temperature microclimate across buckets Kemker, 2013; Ribaudo, Bertrin, Dutartre, 2014), the pres- (Stiers, Njambuya, Triest, 2011). Plant fresh weight was ence and abundance of organisms and organic matter, and measured in grams once every 2 weeks using an Analogue their associated biological processes (e.g. respiration and & Digital EK-300i compact balance scales. Upon removal decomposition) can greatly alter water conditions. Gauze from water buckets (by hand), plant samples were left to drain on the top of a gauze mesh (placed over the bucket) for 1 min per plant to replenish water and prevent inaccur- ate fresh weight readings due to added weight. It was during this stage that the associated pond life, i.e. invertebrate spe- cies, were individually counted and recorded manually. The weighing process presented an opportunity to inspect the plants and water bucket contents, whilst causing the least disturbance to organisms present. Plastic, transparent tubs were used to transfer plant samples from the gauze mesh to the scales and back into their corresponding buckets and also to transfer any organisms found safely to a nearby pond (~10 m away from study site). Figure 1. Satellite map of ponds at Penrose Water Gardens, Truro, Data analysis where C. demersum (A6) and L. major (A8) samples were collected. Dotted black line indicates the boundary point of sample collection; All statistical analyses were carried out in Minitab 17 red bar indicates 25 m (Google Maps, 2016). Statistical Software (2010). ............................................................................................... .................................................................. 3 Downloaded from https://academic.oup.com/biohorizons/article/doi/10.1093/biohorizons/hzy008/5151366 by DeepDyve user on 10 August 2022 Research article Bioscience Horizons � Volume 11 2018 ............................................................................................... .................................................................. to 13 freshwater invertebrate ‘species’ from a single sample Results observation. The DO concentration of the experimental ponds was sig- The fresh weight of the two species differed significantly nificantly affected by treatment (L. major, C. demersum, during the experimental period; L. major samples increased control) over the duration of the experiment (Fig. 2A; gen- by ~16% (Fig. 4; F = 70.3, p = 0.000). However, estab- 7, 42 eral linear methods; treatment: F = 53.4, p < 0.0001; 11, 264 lishment time had no significant effect on fresh weight (Fig. 4; days: F = 11.1, p < 0.001). Whilst the pond tempera- 24, 264 F = 1.5, p = 0.209). 6, 42 ture changed over the course of observations (Fig. 2B; Qualitatively, there was a notable difference, particularly F = 5003.4, p < 0.001), there was no significant effect 24, 264 with L. major, in the appearance of the samples at the start of of treatment (Fig. 2B; F = 1.4, p = 0.160); therefore 11, 264 the experiment compared to the end (Figs 5 and 6). Similarly, temperature effects were not responsible for the DO changes after measurements had ceased and the simulated pond condi- between the treatments. tions were left for a further 2 weeks (17/03/16), there were The pond life abundances associated with native C. striking visual differences between native and non-native demersum ponds were significantly higher than non-native plants. All L. major replicates were in a state of decompos- L. major (Fig. 3; F = 4.6, p = 0.001). Establishment time 7, 42 ition, unlike C. demersum replicates, which appeared to of the plants also had a significant effect on the number of remain in a healthy condition (Fig. 7). invertebrate species present (Fig. 3: F = 3.1, p = 0.013). 6, 42 The pond life associated with L. major and C. demersum (pond life was absent in the control buckets) ranged from 0 Figure 3. Comparison of pond life abundance associated with the native (C. demersum) and non-native (L. major) plants over time. Values are means ± S.E. (n = 4) of the total number counted of all species. The two treatments are indicated by colours and symbols (blue□= L. major, green△ = C. demersum). No pond life was observed in the control buckets. Figure 2. Change in DO (A) and water temperature (B) with time since Figure 4. Change in fresh weight with time since the start of the start of observations. Values are means ± S.E. (n = 4). Three observations. Values are means ± S.E. (n = 4). The two treatments are treatments indicated by colours and symbols (red○ = control, i.e. indicated by symbols and colours (blue□ = L. major, green△ = C. water, blue□ = L. major, green△= C. demersum). demersum). ............................................................................................... .................................................................. 4 Downloaded from https://academic.oup.com/biohorizons/article/doi/10.1093/biohorizons/hzy008/5151366 by DeepDyve user on 10 August 2022 Bioscience Horizons � Volume 11 2018 Research article ............................................................................................... .................................................................. higher levels of DO than L. major (Fig. 2A). Fluctuations in Discussion overall DO concentrations were associated with temperature changes (Figs 2A and B) and were explicable in terms of the This research demonstrates for the first time the oxygenating known effects of temperature on DO; as temperature efficacies, growth rates and associated pond life abundances increases, the solubility of oxygen decreases as gases are typic- of two macrophyte species, native, C. demersum and non- ally more soluble at colder temperatures (Tadesse, Green, native, L. major, established under small-pond conditions. Puhakka, 2004; Desmet et al., 2011; Hussner, Hofstra, Jahns, The results showed significant differences between the species’ 2011; Riis et al., 2012; Kemker, 2013). For example at DO concentrations over time, with C. demersum maintaining around 49, 59, 87 and 115 days from establishment, where mean temperatures reached maxima (13.2°C, 13.3°C, 12.5°C and 10.7°C, respectively), mean DO concentrations of all samples decreased considerably (Fig. 2A). However, as there were no significant differences between the temperatures of the treatments (Fig. 2B), it was clear that temperature was not the cause of the significant DO variations that occurred between the treatments. Ceratophyllum demersum consistently had higher asso- ciated pond life abundance, with a more diverse collection than L. major—often there was no associated biodiversity (Fig. 3). Although little has been published on the preferences Figure 5. Lagarosiphon major (left) and C. demersum (right) samples in and tolerance levels of native fish and invertebrate species for 24-cm-diameter buckets at the start of the experiment (photographs: DO, previous research has documented that the requirement R. Mitchell-Holland, 2016). for most freshwater fish is >6 mg/L, and around 5 mg/L for freshwater insects (Davis, 1975). Wurts (1993) proposed that DO levels <3 mg/L are insufficient to support aquatic life (e.g. fish), with more recent literature (Leppi, Arp, Whitman, 2016), suggesting that many freshwater organisms will be adversely affected when DO falls below a level of 2 mg/L for prolonged periods. Whilst DO reached a maximum of 11.9 mg/L in C. demersum and control buckets over the course of the experiment, one L. major replicate caused DO to fall to a minimum of 1.1 mg/L (Supplementary data, Table 1); this is well below the level which is classed as sus- tainable for most aquatic life. Other L. major replicates often fell below the recommended healthy requirements for native freshwater invertebrates (5 mg/L), with even the mean values Figure 6. Lagarosiphon major (left) and C. demersum (right) samples in 24-cm-diameter buckets at the end of the experiment (photographs: R. (4.5 and 3.9 mg/L) falling to near-lethal levels on several occa- Mitchell-Holland, 2016). sions (Fig. 2A). Oxygen availability is known to be a major Figure 7. Water buckets containing L. major samples (left) and C. demersum (right) 2 weeks post experiment. ............................................................................................... .................................................................. 5 Downloaded from https://academic.oup.com/biohorizons/article/doi/10.1093/biohorizons/hzy008/5151366 by DeepDyve user on 10 August 2022 Research article Bioscience Horizons � Volume 11 2018 ............................................................................................... .................................................................. factor determining the occurrence and abundance of many Martin and Coetzee (2014) found that L. major had a faster aquatic communities (Ruse, 1996; Gabriels et al., 2007; RGR and was overall a superior competitor to M. spicatum. Desmet et al., 2011) as low DO concentrations characterize However, as observed in Ranunculus circinatus by diminished water quality and have adverse effects on asso- Larson (2007) and Myriophyllum spicatum by Angelstein ciated species (Hussner et al., 2014). This can explain why L. et al. (2009), any treatment used for manipulating the plants major consistently had significantly less associated biodiver- (i.e. by hand when weighing) can be a potential stress factor sity than C. demersum— particularly evident in L. major rep- and impose loss of vitality. Thus, this may have influenced licate 1 (Supplementary data, Table 2), which had the lowest the weight differences observed between the two species in mean DO overall (5.4 mg/L) and no associated pond life over this experiment, as well as decomposition and fragmenta- the study period. The significant effect of time on pond life tion. After only a few weeks of establishment, although abundance can also be explained by the significant effect of fragmentation of both species was observed, it was more time on DO, which increased with C. demersum, and decreased apparent in C. demersum samples. By January, one L. major with L. major samples. Across all C. demersum samples, levels replicate (Lm 1) was beginning to decompose and was never fell below 6.4 mg/L throughout the study period, thus, severely decomposed by February. As stated by Rattray, were consistently sustainable for aquatic life. Furthermore, the Howard-Williams, Brown (1994) and Nault and Mikulyuk literature states that certain species may be indicators of water (2009) decomposing mats of L. major create extremely low quality. For example, shrimps (Crangonyx pseudogracilis), oxygen levels in the water, which clarifies the consistently which were only associated with C. demersum samples, are low DO concentrations of that particular sample (lowest often only present in good-quality ponds (Freshwater Habitats DO readings overall—1.1 mg/L). However, these observa- Trust, 2016). Caddis flies, which were abundant in C. demer- tions do not concur with the literature that states that L. sum pond conditions but absent in L. major, and water snails major is effectively perennial (Keenan, Baars, Caffrey, 2009) may mean that the water quality is relatively good (Freshwater as none of the samples survived through the winter and were Habitats Trust, 2016). Water slaters (Asellus aquaticus)and all heavily decomposed by the end of the experiment (Fig. 7). sludge worms (Tubifex tubifex) were the most abundant species This may be because the small, simulated pond conditions are associated with L. major. Such pollution-tolerant species may more susceptible to temperature change, which limits the be indicators of relatively poor water quality (Freshwater ability to extrapolate the results to a natural ecosystem. Habitats Trust, 2016). Overall, these findings demonstrate that Furthermore, although many submerged macrophytes are the native plant was associated with freshwater invertebrates able to tolerate changes in temperature well (Rooney, Kalff, while the non-native plant was not (Supplementary material, Habel, 2003), L. major is thought to be unable to withstand Table 2). temperatures below 10°C, dying or becoming dormant when Outside of its normal growing season, L. major grew exposed (Australia Natural Heritage Trust, 2003; CABI, more than the native species in terms of overall growth, with 2016). Therefore, the mean temperature of 7.29°C over the an end mean weight of 233.1 g compared to the 198.3 g data collection period may have been a contributing factor mean of C. demersum samples. L. major not only increased for the decomposing/dying plants. in fresh weight but also exhibited a wider variability in However, even outside of the species’ usual growth season, growth patterns across replicates, deviating quite far from its and with findings limited by low temperature (considered initial 200 g start-weight at times (Supplementary data, minimal given that its optimum is 20–23°C), L. major grew Table 3). In comparison, C. demersum showed no growth. more (Fig. 4) and caused oxygen depletion. This strongly sug- This indicates that L. major has an ability to be more invasive, gests that the impacts associated with L. major (rapid growth, with high unpredictability in its growth rates, which poses diminished DO) will be exacerbated during its growth season many issues when implementing guidelines in relation to the (Wilcock et al., 1998). Furthermore, although data from the trade and promotion of this species for aquarium and pond on the provisional mean temperature for the UK were below use. The fresh weight findings from this study are in line with the 1981–2010 long-term average, global surface temperate previous research results (Stiers, Njambuya, Triest, 2011; data from NASA (2016) have reached an all-time high, which Martin and Coetzee, 2014). Rattray, Howard-Williams, is predicted to rise. Elevated temperatures and increased light Brown, 1994 revealed that, in comparison to the macrophyte irradiation are likely to significantly increase L. major growth Myriophyllum triphyllum, L. major has a greater ability to rates and heighten invasion risks, further impacting DO and increase both height and fresh weight during the colonization threatening oxygen-dependent organisms (Hussner, Hofstra, stage. A similar study by Stiers, Njambuya, Triest (2011), Jahns, 2011). using a direct comparison of the two species used in this experiment (in similar pond conditions), found that L. major While longitudinal studies conducted on natural ponds outperformed C. demersum in relative growth rate (RGR) over the summer months (typical growth period) are recom- (based on total length and weight) under two different sedi- mended to strengthen the validity of this study’s findings, the ment conditions. More recently, in a comparison of the com- results clearly suggest that invasive non-native L. major has petitive abilities of L. major and Myriophyllum spicatum, detrimental impacts on its freshwater environment. As this ............................................................................................... .................................................................. 6 Downloaded from https://academic.oup.com/biohorizons/article/doi/10.1093/biohorizons/hzy008/5151366 by DeepDyve user on 10 August 2022 Bioscience Horizons � Volume 11 2018 Research article ............................................................................................... .................................................................. Australia Natural Heritage Trust. (2003) Lagarosiphon - Lagarosiphon species was not an efficient oxygenator (quite the opposite of major. Weed Management Guide, Natural Heritage Trust, Australia. its sale title), results could inform current practice and legisla- tion negotiations in relation to the legal trade of L. major in Bowmer, K. H., Jacobs, S. W. L. and Sainty, G. R. (1995) Identification, the UK, offering a safer, more effective alternative (C. demer- biology and management of Elodea canadensis, Hydrocharitaceae, sum) to the aquatic oxygenating plant industry. Journal of Aquatic Plant Management, 33, 13–19. In conclusion, L. major is detrimental to freshwater ecosys- CABI. (2016) Largarosiphon major (African elodea), accessed at: http:// tems, causing DO depletions and creating unfavourable living www.cabi.org/isc/datasheet/30548 (2 April 2016). conditions for pond life, which deteriorates over time. These detriments are likely to be exacerbated during the usual Caffrey, J. M. (1993) Plant management as an integrated part of growth season of L. major, and in the future as a result of glo- Ireland’s aquatic resource, Hydroécologie Appliquée,5, 77–96. bal warming increases. Caffrey, J. M. and Monahan, C. (2006) Control of Myriophyllum verticilla- tum L. in Irish canals by turion removal, Hydrobiologia, 570, 211–215. Supplementary data Caraco, N., Cole, J., Findlay, S. et al. (2006) Vascular plants as engineers Supplementary data are available at BIOHOR online. of oxygen in aquatic systems, Bioscience, 56, 219–225. Carrillo, Y., Guarín, A. and Guillot, G. (2006) Biomass distribution, growth and decay of Egeria densa in a tropical high-mountain reservoir Authors’ biography (NEUSA, Colombia), Aquatic Botany, 85, 7–15. Rhiann Mitchell-Holland attended Cornwall College Newquay CBD (The Convention on Biological Diversity)., Information about GB from 2013 to 2016 and obtained an FdSc in Wildlife Education Non-native Species Risk Assessments, accessed at: file:///Users/ and Media, and a BSc in Applied Zoology. Currently a pre- annettelumb/Downloads/RA_Lagarosiphon_major_(Curly_Waterweed). senter and educator at Newquay Zoo, Cornwall, Rhiann’spar- pdf (2011) (18 November 2015). ticular fields of interest include the risks, prevention and management of invasive non-native species in the UK, wild- Davis, J. C. (1975) Minimal dissolved oxygen requirements of aquatic life management, biodiversity conservation and education, life with emphasis on Canadian species: a review, Journal of the and sustainability. Rhiann aims to apply her skills in research Fisheries Research Board of Canada, 32, 2295–2332. and the development of wildlife/environmental management Desmet, N. J. S., Van Belleghem, S., Seuntjens, P. et al. (2011) and conservation plans to combat current threats and protect Quantification of the impact of macrophytes on oxygen dynamics our biological resources. Rhiann designed the details of the and nitrogen retention in a vegetated lowland river, Physics and study, conducted research, analysed data, wrote the paper Chemistry of the Earth, Parts A/B/C, 36, 479–489. and had primary responsibility for final content. Nicola Morris co-supervised the project (conception and study over- Dudgeon, D., Arthington, A. H., Gessner, M. O. et al. (2006) Freshwater sight) and provided essential materials. Peter McGregor biodiversity: importance, threats, status and conservation chal- co-supervised the project (conception, development, data lenges, Biological Reviews, 81, 163–182. collection and statistical advice and study oversight) and EPA., What are Suspended and Bedded Sediments (SABS)? accessed at: contributed to paper write-up. http://water.epa.gov/scitech/datait/tools/warsss/sabs.cfm (2012) (28 February 2016). Acknowledgements EU. (2016) Commission Implementing Regulation (EU) 2016/1141, accessed at: http://eur-lex.europa.eu/legal-content/EN/TXT/?qid= The authors thank Trevor Renals, Environment Agency and 1468477158043&uri=CELEX:32016R1141 (2016) (8 June 2017). Jonathan Newman, for sharing their expertise and technical advice. European Parliament., Invasive Alien Species (2014), accessed at: http://www.europarl.europa.eu/RegData/etudes/workshop/join/ 2014/518746/IPOL-ENVI_AT(2014)518746_EN.pdf (11 October References 2015). Angelstein, S., Wolfram, C., Rahn, K. et al. (2009) The influence of differ- Freshwater Habitats Trust., Shrimp, accessed at: http://freshwater ent sediment nutrient content on growth and competition of habitats.org.uk/habitats/pond/identifying-creatures-pond/shrimp/ Elodea nuttalli and Myriophyllum spicatum in nutrient-poor waters, (2016) (10 May 2016). Fundamental and Applied Limnology, 175, 49–57. Gabriels, W., Goethals, P. L. M., Dedecker, A. P. et al. (2007) Analysis of Annis, R. B. Water Resources Institute: Dissolved Oxygen, accessed at: macrobenthic communities in Flanders, Belgium, using a stepwise https://www.gvsu.edu/wri/education/instructors-manual-dissolved- input variable selection procedure with artificial neural networks, oxygen-30.htm (2014) (15 March 2015). Aquatic Ecology, 41, 427–441. ............................................................................................... .................................................................. 7 Downloaded from https://academic.oup.com/biohorizons/article/doi/10.1093/biohorizons/hzy008/5151366 by DeepDyve user on 10 August 2022 Research article Bioscience Horizons � Volume 11 2018 ............................................................................................... .................................................................. Google Maps., Penrose Water Gardens, accessed at: https://www. Natural Heritage Trust., Lagarosiphon – Lagarosiphon major. Weed google.co.uk/maps/place/Penrose+Water+Gardens/ (2016) (20 Management Guide. Canberra, Australia: Department of Sustainability, March 2016). Environment, Water, Population and Communities, accessed at: http:// www.weeds.gov.au/publications/guidelines/alert/pubs/l-major.pdf Gray, J. S., Wu, R. S. and Or, Y. Y. (2002) Effects of hypoxia and organic (2003) (6 October 2015). enrichment on the coastal marine environments, Marine Ecological Progress Series, 238, 249–279. Nault, M. E. and Mikulyuk, A. (2009) African Elodea (Lagarosiphon major): A Technical Review of Distribution, Ecology, Impacts, and Hussner, A., Hofstra, D. and Jahns, P. (2011) Diurnal courses of net Management, Wisconsin Department of Natural Resources Bureau photosynthesis and photosystem II quantum efficiency of sub- of Science Services, Madison, Wisconsin, USA. merged Lagarosiphon major under natural light conditions, Flora, 206, 904–909. NNSS., Information about GB Non-native Species Risk Assessments, accessed at: file:///Users/annettelumb/Downloads/RA_Lagarosiphon_ Hussner, A., Hofstra, D., Jahns, P. et al. (2014) Response capacity to CO2 major_(Curly_Waterweed).pdf (2011) (10 March 2015). depletion rather than temperature and light effects explain the growth success of three alien Hydrocharitaceae compared with NNSS., England and Wales: The Countryside Act 1981. Accessed at: native Myriophyllum triphyllum in New Zealand, Aquatic Botany, http://www.nonnativespecies.org//index.cfm?pageid=67 (2016) (2 120, 205–211. January 2016). Kay, K. H. and Hoyle, S. T. (2001) Mail order, the internet, and invasic Paerl, H. W., Fulton, R. S., Moisander, P. M. et al. (2001) Harmful fresh- aquatic Weeds, Journal of aquatic Plant Management, 39, 88–91. water algal blooms, with an emphasis on Cyanobacteria, The Scientific World Journal,1, 76–113. Keenan, E., Baars, J.-R. and Caffrey, J. M. (2009) Changes in littoral inver- tebratecommunities in loughcorribinresponsetoaninvasionby Pimentel, D., Lach, L., Zuniga, R. et al. (2000) Environmental and eco- Lagarosiphon major, in Pieterse A., Rytkonen A.-M. and Hellsten S. nomic costs of nonindigenous species in the United States, (eds), Aquatic Weeds, Finnish Environment Institute, Finland, pp. 24–28. Bioscience, 50, 53–65. Kemker, C., Dissolved Oxygen: Fundamentals of Environmental Rattray, M. R., Howard-Williams, C. and Brown, J. M. (1994) Rates of early Measurements. Fondriest Environmental, accessed at: http://www. growth of propagules of Lagarosiphon major and Myriophyllum tri- fondriest.com/environmental-measurements/parameters/water- phyllum in lakes of differing trophic status, New Zealand Journal of quality/dissolved-oxygen/#2 (2013) (22 February 2016). Marine and Freshwater Research, 28, 235–241. Larson, D. (2007) Growth of three submberged plants below different Ribaudo, C., Bertrin, V. and Dutartre, A. (2014) Dissolved gas and nutri- densities of nymphoides peltara (SG, Gmel) Kuntze, Aquatic Botany, ent dynamics within an Egeria densa Planch. bed, Acta Botanica 86, 280–284. Gallica, 161, 233–241. Lenntech., Why oxygen dissolved in water is important, accessed at: Riis, T., Olsen, B., Clayton, S. J. et al. (2012) Growth and morphology in rela- http://www.lenntech.com/why_the_oxygen_dissolved_is_important. tion to temperature and light availability during the establishment of htm (2015) (27 January 2015). three invasive aquatic plant species, Aquatic Botany, 102, 56–64. Leppi, J. C., Arp, C. D. and Whitman, M. S. (2016) Predicting late winter Rooney, N., Kalff, J. and Habel, C. (2003) The role of submerged macro- dissolved oxygen levels in Arctic lakes using morphology and land- phyte beds in phosphorus and sediment accumulation in Lake scape metrics, Environmental Management, 57, 463–473. Memphremagog, Quebec, Canada, Limnology Oceanography, 48, 1927–1937. Loverde-Oliveira, S. M., Moraes Huszar, V. L., Mazzeo, N. et al. (2009) Hydrology-driven regime shifts in a shallow tropical lake, Royal Horticultural Society., Lagarosiphon major (curly waterweed), Ecosystems, 12, 807–819. accessed at: https://www.rhs.org.uk/Plants/9805/Lagarosiphon- major/Details?returnurl=%2Fplants%2Fsearch-results (2016) (29 Martin, G. D. and Coetzee, J. A. (2014) Competition between two aquatic March 2016). macrophytes, Lagarosiphon major (Ridley) Moss (Hydrocharitaceae) and Myriophyllum spicatum Linnaeus (Haloragaceae) as influenced Ruse, L. P. (1996) Multivariate techniques relating macroinvertebrate by substrate sediment and nutrients, Aquatic Botany,114, 1–11. and environmental data from a river catchment, Water Research, 30, 3017–3024. Mazzeo, N., Rodríguez-Gallego, L., Kruk, C. et al. (2003) Effects of Egeria densa Planch. beds on a shallow lake without piscivorous fish, Sand-Jensen, K. (1989) Environmental variables and their effect on photo- Hydrobiologia, 506 (1), 591–602. synthesis of aquatic plant communities, Aquatic Botany,34, 5–25. McGregor, P. G. and Gourlay, H. (2002) Assessing the Prospects for the Schwarz, A. and Howard-Williams, C. (1993) Aquatic weed bed struc- Biological Control of Lagarosiphon (Lagarosiphon major ture and photosynthesis in two New Zealand lakes, Aquatic Botany, (Hydrocharitaceae)), Department of Conservation, New Zealand. 46, 263–281. NASA., Global temperature. Accessed at: http://climate.nasa.gov/ (2016) Stiers, I., Njambuya, J. and Triest, L. (2011) Competitive abilities of inva- (10 May 2016). sive Lagarosiphon major and native Ceratophyllum demersum in ............................................................................................... .................................................................. 8 Downloaded from https://academic.oup.com/biohorizons/article/doi/10.1093/biohorizons/hzy008/5151366 by DeepDyve user on 10 August 2022 Bioscience Horizons � Volume 11 2018 Research article ............................................................................................... .................................................................. monocultures and mixed cultures in relation to experimental sedi- Westphal, M. I., Browne, M., MacKinnon, K. et al. (2008) The link ment dredging, Aquatic Botany, 95, 61–166. between inter-national trade and the global distribution of invasive alien species, Biological Invasions, 10, 391–398. Strayer, D. L., Lutz, C., Malcom, H. M. et al. (2003) Invertebrate commu- nities associated with a native (Vallisneria americana) and an alien Wilcock, R. J., Nagels, J. W., McBride, G. G. et al. (1998) Characterisation (Trapa natans) macrophyte in a large river, Freshwater Biology, 48, of lowland streams using a single‐station diurnal curve analysis 1938–1949. model with continuous monitoring data for dissolved oxygen and temperature, New Zealand Journal of Marine and Freshwater Tadesse, I., Green, F. B. and Puhakka, J. A. (2004) Seasonal and diurnal Research, 32, 67–79. variations of temperature, pH and dissolved oxygen in advanced integrated wastewater pond system® treating tannery effluent, Wurts, W. A. (1993) Dealing with oxygen depletion in ponds, World Water Research, 38, 645–654. Aquaculture, 24, 108–109. ............................................................................................... .................................................................. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png BioScience Horizons Oxford University Press

A Comparison of the oxygenating differences of invasive non-native Lagarosiphon major and native Ceratophyllum demersum

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Downloaded from https://academic.oup.com/biohorizons/article/doi/10.1093/biohorizons/hzy008/5151366 by DeepDyve user on 10 August 2022 BioscienceHorizons Volume 11 2018 10.1093/biohorizons/hzy008 ............................................................................................ ..................................................................... Research article A Comparison of the oxygenating differences of invasive non-native Lagarosiphon major and native Ceratophyllum demersum Rhiann Mitchell-Holland , Nicola Jane Morris and Peter Kenneth McGregor Centre for Applied Zoology, Cornwall College Newquay, Newquay TR7 2LZ, UK *Corresponding Author: Rhiann Mitchell-Holland. Email: rhiann01@hotmail.com Supervisor: Peter McGregor ............................................................................................ ..................................................................... Native to Southern Africa, Lagarosiphon major is a submerged macrophyte that is recognized as a problematic, invasive non-native species in many countries including the UK. It is widely sold and promoted through the aquarium and water gar- den industry as an ‘efficient oxygenator’ for freshwater systems, irrespective of the absence of evidence to support this statement and evidence of its adverse ecological and economic impacts. A key concern, relating to its rapid growth rate and high fresh weight density, is that L. major can impose self-shading and limitation of photosynthetic and respiratory activity, causing it to consume more oxygen than it produces. Low dissolved oxygen (DO) conditions typify diminished water quality and seriously limit oxygen-dependent organisms. We measured over several months the DO, fresh weight and associated pond life abundances of L. major and a comparable UK-native macrophyte, Ceratophyllum demersum, estab- lished in small-pond conditions to determine which species best maintained a healthy freshwater environment. Both the time from establishment and species had significant effects on DO concentrations and pond life abundance; L. major pro- duced the least amount of oxygen over time and had significantly less associated pond life compared to the native plant. L. major also increased significantly in overall fresh weight compared to C. demersum, indicating the higher invasive ability of the non-native species. In conclusion, our results suggest that L. major is not as good an oxygenator as C. demersum and that this native species should be promoted through the aquarium and water garden trades as an efficient oxygenator that improves water quality and habitat conditions over time. Key words: invasive non-native species, macrophytes, dissolved oxygen, pond life, fresh weight, water quality Submitted on 24 October 2017; editorial decision on 10 September 2018 ............................................................................................ ..................................................................... Strayer et al., 2003; Dudgeon et al., 2006; Riis et al., 2012). Introduction In cases where such plants have outcompeted and replaced As a result of worldwide travel and trade, numerous invasive native submerged vegetation (Rattray, Howard-Williams, species have been introduced, both intentionally and inadvert- Brown, 1994; Keenan, Baars, Caffrey, 2009), severe depletion ently, into areas beyond their natural range (Westphal et al., of dissolved oxygen (DO) and diminished water quality has 2008; Stiers, Njambuya, Triest, 2011). Aquatic plant species been the result (Caraco et al., 2006; Leppi, Arp, Whitman, invasion has been recognized as one of the largest threats to 2016). Organisms, such as freshwater fish, invertebrates, freshwater ecosystems and biodiversity, with detrimental con- plants and bacteria, rely on DO (the level of free, non- sequences for ecology and the economy (Pimentel et al., 2000; compound oxygen present in water) for survival, thus cannot ............................................................................................... .................................................................. © The Author(s) 2018. Published by Oxford University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. Downloaded from https://academic.oup.com/biohorizons/article/doi/10.1093/biohorizons/hzy008/5151366 by DeepDyve user on 10 August 2022 Research article Bioscience Horizons � Volume 11 2018 ............................................................................................... .................................................................. withstand anoxic (a total depletion of oxygen) or even hyp- pH values that create further complications for many aquatic oxic (low oxygen) conditions for extended periods of time vertebrate and invertebrate species (Sand-Jensen, 1989; (Gray, Wu, Or, 2002; Caraco et al., 2006; Lenntech, 2015). Hussner et al., 2014). Due to the decidedly invasive nature of The presence and abundance of organisms and organic mat- L. major, which has already been banned in New Zealand ter (and their associated biological processes) can greatly and Australia (Natural Heritage Trust, 2003), it is an offence influence DO concentrations in a body of water (Caraco to plant or otherwise allow this species to grow in the wild in et al., 2006; Desmet et al., 2011; Kemker, 2013; Ribaudo, the UK, under Schedule 9 of the Wildlife and Countryside Bertrin, Dutartre, 2014). For example, while photosynthesis Act (NNSS, 2016). However, natural checks on the growth contributes to an increase in DO (Desmet et al., 2011), the of L. major in the UK are insufficient, and control/eradica- process of respiration by organisms, and decomposition of tion of the species is extremely costly and often ineffective organic matter by microorganisms, can severely deplete the (Caffrey, 1993; Caffrey and Monahan, 2006; Stiers, available DO for aerobic species (Caraco et al., 2006; Njambuya, Triest, 2011; European Parliament, 2014). Desmet et al., 2011; EPA, 2012; Annis, 2014). Despite high Despite its environmental, ecological and economic DO productivity during the day (Carrillo, Guarín, Guillot, impacts, L. major is a popular water garden/aquarium plant, 2006; Ribaudo, Bertrin, Dutartre, 2014), dense clusters of often sold as Egeria or Elodea densa through the aquatics aquatic plants can cause water hypoxia at night, particularly industry (NNSS, 2011; J. Newman, personal communica- in slow-moving water bodies, as the rate of oxygen con- tion). The UK population of L. major has been intentionally sumption at the lower level of the bed cannot be replenished planted as an ‘oxygenator’ and is often promoted through the by diffusion from the atmosphere (Mazzeo et al., 2003; trade as one of the best (Natural Heritage Trust, 2003; Nault Loverde-Oliveira et al., 2009). Quantifying the impact of and Mikulyuk, 2009; CBD, 2011; CABI, 2016; Royal abundant macrophytes on basic water quality (oxygen Horticultural Society, 2016). Its English common name ‘oxy- dynamics, nitrogen retention and nutrient concentrations), gen weed’—referring to the species’ ability to add oxygen to Desmet et al. (2011) found that diurnal and seasonal fluctua- the water as a result of its high photosynthetic rate (Rattray, tions of DO were strongly correlated with plant growth/bio- Howard-Williams, Brown, 1994; CABI, 2016)—is the likely mass density, temperature and solar irradiance, observing reason behind the industry’s promotion of the plant. water hypoxia during the summer. Since light and tempera- However, the high biomass densities that are characteristic of ture are triggers for biological processes, these diurnal and this macrophyte are likely to lead to a higher consumption seasonal shifts can be affected by climatological conditions; than production of oxygen, seriously limiting other aquatic such findings match literature knowledge about the impacts of species (Natural Heritage Trust, 2003; Nault and Mikulyuk, dominating macrophytes on DO dynamics (Natural Heritage 2009). The trade of this plant as an ornamental through the Trust, 2003; Tadesse, Green, Puhakka, 2004; Hussner, Internet and mail order greatly increases its obtainability and Hofstra, Jahns, 2011; Riis et al.,2012). ease of spread to new locations (Kay and Hoyle, 2001; An invasive non-native species of particular concern is Australia Natural Heritage Trust, 2003; CABI, 2016). Lagarosiphon major (Ridley) Moss. L (Hydrocharitaceae). Much of the existing literature regarding L. major focuses Native to South Africa, this submerged macrophyte is a con- on the core factors affecting aquatic plant growth and siderable potential threat to static water bodies in many morphology, such as temperature/light conditions (Desmet countries, including the UK, where it is now well established et al., 2011; Riis et al., 2012), availability of carbon and (Bowmer, Jacobs, Sainty, 1995; NNSS, 2011; J. Newman, nutrients (Hussner et al., 2014)orcompetitive abilities personal communication). In addition to the aforementioned (Stiers, Njambuya, Triest, 2011; Martin and Coetzee, 2014). problems associated with aquatic plant species invasion, L. However, little attention has been paid primarily to the oxy- major has been observed forming dense canopies that often genating abilities of L. major, with seemingly no existing lit- occupy entire water volumes of slow-moving water bodies erature that directly measures its effects on DO over time. (Stiers, Njambuya, Triest, 2011). These thick mats block Thus, in addition to filling this gap in the literature, our light penetration to other flora (eliminating their growth), study aimed to compare L. major as an oxygenator with the restrict water movement and interfere with recreation activ- UK-native macrophyte, Ceratophyllum demersum (rigid ities, ultimately exacerbating flood risks (Schwarz and hornwort). C. demersum was chosen based on its similar Howard-Williams, 1993; McGregor and Gourlay, 2002; morphological and growth characteristics to L. major. Stiers, Njambuya, Triest, 2011). Ceratophyllum demersum is also widely sold as an oxygen- As with other aquatic invasive species, L. major outcom- ating plant and is recognized as invasive outside of its nat- petes native aquatic vegetation and affects associated popula- ural range, although it does not share as many of the tions of species as it has a rapid growth rate and is effectively inherent risks as L. major (McGregor and Gourlay, 2002). perennial, surviving through the winter (Keenan, Baars, Our experiment also measured and compared the differences Caffrey, 2009; NNSS, 2011; J. Newman, personal communi- in growth (fresh weight) and associated pond life abundance cation). Furthermore, it is effective at removing CO and and diversity of the two species over 12 weeks to assess their HCO − from water via photosynthesis, resulting in very high invasiveness and habitat impact. ............................................................................................... .................................................................. 2 Downloaded from https://academic.oup.com/biohorizons/article/doi/10.1093/biohorizons/hzy008/5151366 by DeepDyve user on 10 August 2022 Bioscience Horizons � Volume 11 2018 Research article ............................................................................................... .................................................................. mesh coverings were considered to exclude organisms and Materials and Methods organic matter. However, in order to retain natural light irradiance and temperature of the water, and in turn Plant sample collection strengthen the integrity of the experiment (since contamin- Healthy plant samples of C. demersum (800 g) and L. major ation is a natural occurrence in ponds), the buckets were (800 g) were collected from two adjacent ponds (A6 and A8) instead, monitored daily for major debris contamination at Penrose Water Gardens, Truro Cornwall (Fig. 1)on 7 (floating leaves, dead insects, etc.); anything found was October 2015. As pond A8 was larger than pond A6, samples removed with a sieve promptly. were only collected within an area of similar size to pond A6 (boundary indicated by dotted line, Fig. 1), ensuring that both Parameters measured species derived from similar depth, light, temperature and Six weeks after establishment, DO (mg/L) and temperature growth conditions to limit the degree of variation in morph- (°C) of the water in each bucket were measured twice a week ology. Samples were collected with a rake and by hand from for 12 weeks (10 December 2015–3 March 2016) using randomly selected areas of the two ponds, avoiding sample Hanna Instruments (Leighton Buzzard, UK) HI9142 portable selection bias and retaining sample independence. All samples waterproof DO meter and a TPI-315C (Crawley, UK) digital were rinsed thoroughly on site (within ponds), and again later thermometer. Data collection always began at 1 h and 20 min with settled tap water, to ensure no invertebrates or other after sunrise to control for diurnal effects on DO (informed plant species were present; any found were returned to their by pilot study, personal observation) and collected in a respective ponds, or a nearby garden pond at the study site. balanced order to limit the degree of variation between buck- ets over time. The DO meter was left for 15 min before any Experimental setup measurements were taken to allow time for equilibration (fol- The experiment was conducted outdoors in Truro, Cornwall, lowing manufacturer’s recommendations), and a 1-min per between October 2015 and March 2016. Simulating small- bucket time limit was allocated for DO and temperature read- pond conditions, 200 g of L. major and 200 g of C. demersum ings. Along with DO and temperature parameters, the date, of similar size and root length were placed into plastic buckets hours since sunrise, general weather conditions (by visual containing 8 L of settled tap water. Tap water was left to inspection) and water volumes of each bucket were also stand for over 48 h prior to plant introduction (following recorded. Water levels were controlled every other day and Stiers, Njambuya, Triest, 2011) and had a mean (±S.E.) DO kept at ~8000 cm per bucket. If a significant amount of water of 9.6 (±0.049) mg/L; thus simulated pond conditions were was lost or gained as a result of condensation or rainfall (i.e. similar at the start of the experiment. In total, 12 buckets— ±>5cm of original volume), it was replaced with settled tap four replicates of each species and four containing only water water, or removed in order to keep conditions the same, and as controls—were left to establish for 6 weeks (from 29 reduced the potential of algal growth or algae bloom through October 2015 to 10 December 2016) before any measure- water replenishment (Paerl et al., 2001; Stiers, Njambuya, ments were taken. All buckets were situated on a raised Triest, 2011). Buckets were rearranged every other day, decked area ~0.5 m above ground level. As highlighted by again, in a balanced order, to reduce the effects of variation many researchers (Caraco et al., 2006; Desmet et al., 2011; of light and temperature microclimate across buckets Kemker, 2013; Ribaudo, Bertrin, Dutartre, 2014), the pres- (Stiers, Njambuya, Triest, 2011). Plant fresh weight was ence and abundance of organisms and organic matter, and measured in grams once every 2 weeks using an Analogue their associated biological processes (e.g. respiration and & Digital EK-300i compact balance scales. Upon removal decomposition) can greatly alter water conditions. Gauze from water buckets (by hand), plant samples were left to drain on the top of a gauze mesh (placed over the bucket) for 1 min per plant to replenish water and prevent inaccur- ate fresh weight readings due to added weight. It was during this stage that the associated pond life, i.e. invertebrate spe- cies, were individually counted and recorded manually. The weighing process presented an opportunity to inspect the plants and water bucket contents, whilst causing the least disturbance to organisms present. Plastic, transparent tubs were used to transfer plant samples from the gauze mesh to the scales and back into their corresponding buckets and also to transfer any organisms found safely to a nearby pond (~10 m away from study site). Figure 1. Satellite map of ponds at Penrose Water Gardens, Truro, Data analysis where C. demersum (A6) and L. major (A8) samples were collected. Dotted black line indicates the boundary point of sample collection; All statistical analyses were carried out in Minitab 17 red bar indicates 25 m (Google Maps, 2016). Statistical Software (2010). ............................................................................................... .................................................................. 3 Downloaded from https://academic.oup.com/biohorizons/article/doi/10.1093/biohorizons/hzy008/5151366 by DeepDyve user on 10 August 2022 Research article Bioscience Horizons � Volume 11 2018 ............................................................................................... .................................................................. to 13 freshwater invertebrate ‘species’ from a single sample Results observation. The DO concentration of the experimental ponds was sig- The fresh weight of the two species differed significantly nificantly affected by treatment (L. major, C. demersum, during the experimental period; L. major samples increased control) over the duration of the experiment (Fig. 2A; gen- by ~16% (Fig. 4; F = 70.3, p = 0.000). However, estab- 7, 42 eral linear methods; treatment: F = 53.4, p < 0.0001; 11, 264 lishment time had no significant effect on fresh weight (Fig. 4; days: F = 11.1, p < 0.001). Whilst the pond tempera- 24, 264 F = 1.5, p = 0.209). 6, 42 ture changed over the course of observations (Fig. 2B; Qualitatively, there was a notable difference, particularly F = 5003.4, p < 0.001), there was no significant effect 24, 264 with L. major, in the appearance of the samples at the start of of treatment (Fig. 2B; F = 1.4, p = 0.160); therefore 11, 264 the experiment compared to the end (Figs 5 and 6). Similarly, temperature effects were not responsible for the DO changes after measurements had ceased and the simulated pond condi- between the treatments. tions were left for a further 2 weeks (17/03/16), there were The pond life abundances associated with native C. striking visual differences between native and non-native demersum ponds were significantly higher than non-native plants. All L. major replicates were in a state of decompos- L. major (Fig. 3; F = 4.6, p = 0.001). Establishment time 7, 42 ition, unlike C. demersum replicates, which appeared to of the plants also had a significant effect on the number of remain in a healthy condition (Fig. 7). invertebrate species present (Fig. 3: F = 3.1, p = 0.013). 6, 42 The pond life associated with L. major and C. demersum (pond life was absent in the control buckets) ranged from 0 Figure 3. Comparison of pond life abundance associated with the native (C. demersum) and non-native (L. major) plants over time. Values are means ± S.E. (n = 4) of the total number counted of all species. The two treatments are indicated by colours and symbols (blue□= L. major, green△ = C. demersum). No pond life was observed in the control buckets. Figure 2. Change in DO (A) and water temperature (B) with time since Figure 4. Change in fresh weight with time since the start of the start of observations. Values are means ± S.E. (n = 4). Three observations. Values are means ± S.E. (n = 4). The two treatments are treatments indicated by colours and symbols (red○ = control, i.e. indicated by symbols and colours (blue□ = L. major, green△ = C. water, blue□ = L. major, green△= C. demersum). demersum). ............................................................................................... .................................................................. 4 Downloaded from https://academic.oup.com/biohorizons/article/doi/10.1093/biohorizons/hzy008/5151366 by DeepDyve user on 10 August 2022 Bioscience Horizons � Volume 11 2018 Research article ............................................................................................... .................................................................. higher levels of DO than L. major (Fig. 2A). Fluctuations in Discussion overall DO concentrations were associated with temperature changes (Figs 2A and B) and were explicable in terms of the This research demonstrates for the first time the oxygenating known effects of temperature on DO; as temperature efficacies, growth rates and associated pond life abundances increases, the solubility of oxygen decreases as gases are typic- of two macrophyte species, native, C. demersum and non- ally more soluble at colder temperatures (Tadesse, Green, native, L. major, established under small-pond conditions. Puhakka, 2004; Desmet et al., 2011; Hussner, Hofstra, Jahns, The results showed significant differences between the species’ 2011; Riis et al., 2012; Kemker, 2013). For example at DO concentrations over time, with C. demersum maintaining around 49, 59, 87 and 115 days from establishment, where mean temperatures reached maxima (13.2°C, 13.3°C, 12.5°C and 10.7°C, respectively), mean DO concentrations of all samples decreased considerably (Fig. 2A). However, as there were no significant differences between the temperatures of the treatments (Fig. 2B), it was clear that temperature was not the cause of the significant DO variations that occurred between the treatments. Ceratophyllum demersum consistently had higher asso- ciated pond life abundance, with a more diverse collection than L. major—often there was no associated biodiversity (Fig. 3). Although little has been published on the preferences Figure 5. Lagarosiphon major (left) and C. demersum (right) samples in and tolerance levels of native fish and invertebrate species for 24-cm-diameter buckets at the start of the experiment (photographs: DO, previous research has documented that the requirement R. Mitchell-Holland, 2016). for most freshwater fish is >6 mg/L, and around 5 mg/L for freshwater insects (Davis, 1975). Wurts (1993) proposed that DO levels <3 mg/L are insufficient to support aquatic life (e.g. fish), with more recent literature (Leppi, Arp, Whitman, 2016), suggesting that many freshwater organisms will be adversely affected when DO falls below a level of 2 mg/L for prolonged periods. Whilst DO reached a maximum of 11.9 mg/L in C. demersum and control buckets over the course of the experiment, one L. major replicate caused DO to fall to a minimum of 1.1 mg/L (Supplementary data, Table 1); this is well below the level which is classed as sus- tainable for most aquatic life. Other L. major replicates often fell below the recommended healthy requirements for native freshwater invertebrates (5 mg/L), with even the mean values Figure 6. Lagarosiphon major (left) and C. demersum (right) samples in 24-cm-diameter buckets at the end of the experiment (photographs: R. (4.5 and 3.9 mg/L) falling to near-lethal levels on several occa- Mitchell-Holland, 2016). sions (Fig. 2A). Oxygen availability is known to be a major Figure 7. Water buckets containing L. major samples (left) and C. demersum (right) 2 weeks post experiment. ............................................................................................... .................................................................. 5 Downloaded from https://academic.oup.com/biohorizons/article/doi/10.1093/biohorizons/hzy008/5151366 by DeepDyve user on 10 August 2022 Research article Bioscience Horizons � Volume 11 2018 ............................................................................................... .................................................................. factor determining the occurrence and abundance of many Martin and Coetzee (2014) found that L. major had a faster aquatic communities (Ruse, 1996; Gabriels et al., 2007; RGR and was overall a superior competitor to M. spicatum. Desmet et al., 2011) as low DO concentrations characterize However, as observed in Ranunculus circinatus by diminished water quality and have adverse effects on asso- Larson (2007) and Myriophyllum spicatum by Angelstein ciated species (Hussner et al., 2014). This can explain why L. et al. (2009), any treatment used for manipulating the plants major consistently had significantly less associated biodiver- (i.e. by hand when weighing) can be a potential stress factor sity than C. demersum— particularly evident in L. major rep- and impose loss of vitality. Thus, this may have influenced licate 1 (Supplementary data, Table 2), which had the lowest the weight differences observed between the two species in mean DO overall (5.4 mg/L) and no associated pond life over this experiment, as well as decomposition and fragmenta- the study period. The significant effect of time on pond life tion. After only a few weeks of establishment, although abundance can also be explained by the significant effect of fragmentation of both species was observed, it was more time on DO, which increased with C. demersum, and decreased apparent in C. demersum samples. By January, one L. major with L. major samples. Across all C. demersum samples, levels replicate (Lm 1) was beginning to decompose and was never fell below 6.4 mg/L throughout the study period, thus, severely decomposed by February. As stated by Rattray, were consistently sustainable for aquatic life. Furthermore, the Howard-Williams, Brown (1994) and Nault and Mikulyuk literature states that certain species may be indicators of water (2009) decomposing mats of L. major create extremely low quality. For example, shrimps (Crangonyx pseudogracilis), oxygen levels in the water, which clarifies the consistently which were only associated with C. demersum samples, are low DO concentrations of that particular sample (lowest often only present in good-quality ponds (Freshwater Habitats DO readings overall—1.1 mg/L). However, these observa- Trust, 2016). Caddis flies, which were abundant in C. demer- tions do not concur with the literature that states that L. sum pond conditions but absent in L. major, and water snails major is effectively perennial (Keenan, Baars, Caffrey, 2009) may mean that the water quality is relatively good (Freshwater as none of the samples survived through the winter and were Habitats Trust, 2016). Water slaters (Asellus aquaticus)and all heavily decomposed by the end of the experiment (Fig. 7). sludge worms (Tubifex tubifex) were the most abundant species This may be because the small, simulated pond conditions are associated with L. major. Such pollution-tolerant species may more susceptible to temperature change, which limits the be indicators of relatively poor water quality (Freshwater ability to extrapolate the results to a natural ecosystem. Habitats Trust, 2016). Overall, these findings demonstrate that Furthermore, although many submerged macrophytes are the native plant was associated with freshwater invertebrates able to tolerate changes in temperature well (Rooney, Kalff, while the non-native plant was not (Supplementary material, Habel, 2003), L. major is thought to be unable to withstand Table 2). temperatures below 10°C, dying or becoming dormant when Outside of its normal growing season, L. major grew exposed (Australia Natural Heritage Trust, 2003; CABI, more than the native species in terms of overall growth, with 2016). Therefore, the mean temperature of 7.29°C over the an end mean weight of 233.1 g compared to the 198.3 g data collection period may have been a contributing factor mean of C. demersum samples. L. major not only increased for the decomposing/dying plants. in fresh weight but also exhibited a wider variability in However, even outside of the species’ usual growth season, growth patterns across replicates, deviating quite far from its and with findings limited by low temperature (considered initial 200 g start-weight at times (Supplementary data, minimal given that its optimum is 20–23°C), L. major grew Table 3). In comparison, C. demersum showed no growth. more (Fig. 4) and caused oxygen depletion. This strongly sug- This indicates that L. major has an ability to be more invasive, gests that the impacts associated with L. major (rapid growth, with high unpredictability in its growth rates, which poses diminished DO) will be exacerbated during its growth season many issues when implementing guidelines in relation to the (Wilcock et al., 1998). Furthermore, although data from the trade and promotion of this species for aquarium and pond on the provisional mean temperature for the UK were below use. The fresh weight findings from this study are in line with the 1981–2010 long-term average, global surface temperate previous research results (Stiers, Njambuya, Triest, 2011; data from NASA (2016) have reached an all-time high, which Martin and Coetzee, 2014). Rattray, Howard-Williams, is predicted to rise. Elevated temperatures and increased light Brown, 1994 revealed that, in comparison to the macrophyte irradiation are likely to significantly increase L. major growth Myriophyllum triphyllum, L. major has a greater ability to rates and heighten invasion risks, further impacting DO and increase both height and fresh weight during the colonization threatening oxygen-dependent organisms (Hussner, Hofstra, stage. A similar study by Stiers, Njambuya, Triest (2011), Jahns, 2011). using a direct comparison of the two species used in this experiment (in similar pond conditions), found that L. major While longitudinal studies conducted on natural ponds outperformed C. demersum in relative growth rate (RGR) over the summer months (typical growth period) are recom- (based on total length and weight) under two different sedi- mended to strengthen the validity of this study’s findings, the ment conditions. More recently, in a comparison of the com- results clearly suggest that invasive non-native L. major has petitive abilities of L. major and Myriophyllum spicatum, detrimental impacts on its freshwater environment. As this ............................................................................................... .................................................................. 6 Downloaded from https://academic.oup.com/biohorizons/article/doi/10.1093/biohorizons/hzy008/5151366 by DeepDyve user on 10 August 2022 Bioscience Horizons � Volume 11 2018 Research article ............................................................................................... .................................................................. Australia Natural Heritage Trust. (2003) Lagarosiphon - Lagarosiphon species was not an efficient oxygenator (quite the opposite of major. Weed Management Guide, Natural Heritage Trust, Australia. its sale title), results could inform current practice and legisla- tion negotiations in relation to the legal trade of L. major in Bowmer, K. H., Jacobs, S. W. L. and Sainty, G. R. (1995) Identification, the UK, offering a safer, more effective alternative (C. demer- biology and management of Elodea canadensis, Hydrocharitaceae, sum) to the aquatic oxygenating plant industry. Journal of Aquatic Plant Management, 33, 13–19. In conclusion, L. major is detrimental to freshwater ecosys- CABI. (2016) Largarosiphon major (African elodea), accessed at: http:// tems, causing DO depletions and creating unfavourable living www.cabi.org/isc/datasheet/30548 (2 April 2016). conditions for pond life, which deteriorates over time. These detriments are likely to be exacerbated during the usual Caffrey, J. M. (1993) Plant management as an integrated part of growth season of L. major, and in the future as a result of glo- Ireland’s aquatic resource, Hydroécologie Appliquée,5, 77–96. bal warming increases. Caffrey, J. M. and Monahan, C. (2006) Control of Myriophyllum verticilla- tum L. in Irish canals by turion removal, Hydrobiologia, 570, 211–215. Supplementary data Caraco, N., Cole, J., Findlay, S. et al. (2006) Vascular plants as engineers Supplementary data are available at BIOHOR online. of oxygen in aquatic systems, Bioscience, 56, 219–225. Carrillo, Y., Guarín, A. and Guillot, G. (2006) Biomass distribution, growth and decay of Egeria densa in a tropical high-mountain reservoir Authors’ biography (NEUSA, Colombia), Aquatic Botany, 85, 7–15. Rhiann Mitchell-Holland attended Cornwall College Newquay CBD (The Convention on Biological Diversity)., Information about GB from 2013 to 2016 and obtained an FdSc in Wildlife Education Non-native Species Risk Assessments, accessed at: file:///Users/ and Media, and a BSc in Applied Zoology. Currently a pre- annettelumb/Downloads/RA_Lagarosiphon_major_(Curly_Waterweed). senter and educator at Newquay Zoo, Cornwall, Rhiann’spar- pdf (2011) (18 November 2015). ticular fields of interest include the risks, prevention and management of invasive non-native species in the UK, wild- Davis, J. C. (1975) Minimal dissolved oxygen requirements of aquatic life management, biodiversity conservation and education, life with emphasis on Canadian species: a review, Journal of the and sustainability. Rhiann aims to apply her skills in research Fisheries Research Board of Canada, 32, 2295–2332. and the development of wildlife/environmental management Desmet, N. J. S., Van Belleghem, S., Seuntjens, P. et al. (2011) and conservation plans to combat current threats and protect Quantification of the impact of macrophytes on oxygen dynamics our biological resources. Rhiann designed the details of the and nitrogen retention in a vegetated lowland river, Physics and study, conducted research, analysed data, wrote the paper Chemistry of the Earth, Parts A/B/C, 36, 479–489. and had primary responsibility for final content. Nicola Morris co-supervised the project (conception and study over- Dudgeon, D., Arthington, A. H., Gessner, M. O. et al. (2006) Freshwater sight) and provided essential materials. Peter McGregor biodiversity: importance, threats, status and conservation chal- co-supervised the project (conception, development, data lenges, Biological Reviews, 81, 163–182. collection and statistical advice and study oversight) and EPA., What are Suspended and Bedded Sediments (SABS)? accessed at: contributed to paper write-up. http://water.epa.gov/scitech/datait/tools/warsss/sabs.cfm (2012) (28 February 2016). Acknowledgements EU. (2016) Commission Implementing Regulation (EU) 2016/1141, accessed at: http://eur-lex.europa.eu/legal-content/EN/TXT/?qid= The authors thank Trevor Renals, Environment Agency and 1468477158043&uri=CELEX:32016R1141 (2016) (8 June 2017). Jonathan Newman, for sharing their expertise and technical advice. European Parliament., Invasive Alien Species (2014), accessed at: http://www.europarl.europa.eu/RegData/etudes/workshop/join/ 2014/518746/IPOL-ENVI_AT(2014)518746_EN.pdf (11 October References 2015). Angelstein, S., Wolfram, C., Rahn, K. et al. (2009) The influence of differ- Freshwater Habitats Trust., Shrimp, accessed at: http://freshwater ent sediment nutrient content on growth and competition of habitats.org.uk/habitats/pond/identifying-creatures-pond/shrimp/ Elodea nuttalli and Myriophyllum spicatum in nutrient-poor waters, (2016) (10 May 2016). Fundamental and Applied Limnology, 175, 49–57. Gabriels, W., Goethals, P. L. M., Dedecker, A. P. et al. (2007) Analysis of Annis, R. B. Water Resources Institute: Dissolved Oxygen, accessed at: macrobenthic communities in Flanders, Belgium, using a stepwise https://www.gvsu.edu/wri/education/instructors-manual-dissolved- input variable selection procedure with artificial neural networks, oxygen-30.htm (2014) (15 March 2015). Aquatic Ecology, 41, 427–441. ............................................................................................... .................................................................. 7 Downloaded from https://academic.oup.com/biohorizons/article/doi/10.1093/biohorizons/hzy008/5151366 by DeepDyve user on 10 August 2022 Research article Bioscience Horizons � Volume 11 2018 ............................................................................................... .................................................................. Google Maps., Penrose Water Gardens, accessed at: https://www. Natural Heritage Trust., Lagarosiphon – Lagarosiphon major. Weed google.co.uk/maps/place/Penrose+Water+Gardens/ (2016) (20 Management Guide. Canberra, Australia: Department of Sustainability, March 2016). Environment, Water, Population and Communities, accessed at: http:// www.weeds.gov.au/publications/guidelines/alert/pubs/l-major.pdf Gray, J. S., Wu, R. S. and Or, Y. Y. (2002) Effects of hypoxia and organic (2003) (6 October 2015). enrichment on the coastal marine environments, Marine Ecological Progress Series, 238, 249–279. Nault, M. E. and Mikulyuk, A. (2009) African Elodea (Lagarosiphon major): A Technical Review of Distribution, Ecology, Impacts, and Hussner, A., Hofstra, D. and Jahns, P. (2011) Diurnal courses of net Management, Wisconsin Department of Natural Resources Bureau photosynthesis and photosystem II quantum efficiency of sub- of Science Services, Madison, Wisconsin, USA. merged Lagarosiphon major under natural light conditions, Flora, 206, 904–909. NNSS., Information about GB Non-native Species Risk Assessments, accessed at: file:///Users/annettelumb/Downloads/RA_Lagarosiphon_ Hussner, A., Hofstra, D., Jahns, P. et al. (2014) Response capacity to CO2 major_(Curly_Waterweed).pdf (2011) (10 March 2015). depletion rather than temperature and light effects explain the growth success of three alien Hydrocharitaceae compared with NNSS., England and Wales: The Countryside Act 1981. Accessed at: native Myriophyllum triphyllum in New Zealand, Aquatic Botany, http://www.nonnativespecies.org//index.cfm?pageid=67 (2016) (2 120, 205–211. January 2016). Kay, K. H. and Hoyle, S. T. (2001) Mail order, the internet, and invasic Paerl, H. W., Fulton, R. S., Moisander, P. M. et al. (2001) Harmful fresh- aquatic Weeds, Journal of aquatic Plant Management, 39, 88–91. water algal blooms, with an emphasis on Cyanobacteria, The Scientific World Journal,1, 76–113. Keenan, E., Baars, J.-R. and Caffrey, J. M. (2009) Changes in littoral inver- tebratecommunities in loughcorribinresponsetoaninvasionby Pimentel, D., Lach, L., Zuniga, R. et al. (2000) Environmental and eco- Lagarosiphon major, in Pieterse A., Rytkonen A.-M. and Hellsten S. nomic costs of nonindigenous species in the United States, (eds), Aquatic Weeds, Finnish Environment Institute, Finland, pp. 24–28. Bioscience, 50, 53–65. Kemker, C., Dissolved Oxygen: Fundamentals of Environmental Rattray, M. R., Howard-Williams, C. and Brown, J. M. (1994) Rates of early Measurements. Fondriest Environmental, accessed at: http://www. growth of propagules of Lagarosiphon major and Myriophyllum tri- fondriest.com/environmental-measurements/parameters/water- phyllum in lakes of differing trophic status, New Zealand Journal of quality/dissolved-oxygen/#2 (2013) (22 February 2016). Marine and Freshwater Research, 28, 235–241. Larson, D. (2007) Growth of three submberged plants below different Ribaudo, C., Bertrin, V. and Dutartre, A. (2014) Dissolved gas and nutri- densities of nymphoides peltara (SG, Gmel) Kuntze, Aquatic Botany, ent dynamics within an Egeria densa Planch. bed, Acta Botanica 86, 280–284. Gallica, 161, 233–241. Lenntech., Why oxygen dissolved in water is important, accessed at: Riis, T., Olsen, B., Clayton, S. J. et al. (2012) Growth and morphology in rela- http://www.lenntech.com/why_the_oxygen_dissolved_is_important. tion to temperature and light availability during the establishment of htm (2015) (27 January 2015). three invasive aquatic plant species, Aquatic Botany, 102, 56–64. Leppi, J. C., Arp, C. D. and Whitman, M. S. (2016) Predicting late winter Rooney, N., Kalff, J. and Habel, C. (2003) The role of submerged macro- dissolved oxygen levels in Arctic lakes using morphology and land- phyte beds in phosphorus and sediment accumulation in Lake scape metrics, Environmental Management, 57, 463–473. Memphremagog, Quebec, Canada, Limnology Oceanography, 48, 1927–1937. Loverde-Oliveira, S. M., Moraes Huszar, V. L., Mazzeo, N. et al. (2009) Hydrology-driven regime shifts in a shallow tropical lake, Royal Horticultural Society., Lagarosiphon major (curly waterweed), Ecosystems, 12, 807–819. accessed at: https://www.rhs.org.uk/Plants/9805/Lagarosiphon- major/Details?returnurl=%2Fplants%2Fsearch-results (2016) (29 Martin, G. D. and Coetzee, J. A. (2014) Competition between two aquatic March 2016). macrophytes, Lagarosiphon major (Ridley) Moss (Hydrocharitaceae) and Myriophyllum spicatum Linnaeus (Haloragaceae) as influenced Ruse, L. P. (1996) Multivariate techniques relating macroinvertebrate by substrate sediment and nutrients, Aquatic Botany,114, 1–11. and environmental data from a river catchment, Water Research, 30, 3017–3024. Mazzeo, N., Rodríguez-Gallego, L., Kruk, C. et al. (2003) Effects of Egeria densa Planch. beds on a shallow lake without piscivorous fish, Sand-Jensen, K. (1989) Environmental variables and their effect on photo- Hydrobiologia, 506 (1), 591–602. synthesis of aquatic plant communities, Aquatic Botany,34, 5–25. McGregor, P. G. and Gourlay, H. (2002) Assessing the Prospects for the Schwarz, A. and Howard-Williams, C. (1993) Aquatic weed bed struc- Biological Control of Lagarosiphon (Lagarosiphon major ture and photosynthesis in two New Zealand lakes, Aquatic Botany, (Hydrocharitaceae)), Department of Conservation, New Zealand. 46, 263–281. NASA., Global temperature. Accessed at: http://climate.nasa.gov/ (2016) Stiers, I., Njambuya, J. and Triest, L. (2011) Competitive abilities of inva- (10 May 2016). sive Lagarosiphon major and native Ceratophyllum demersum in ............................................................................................... .................................................................. 8 Downloaded from https://academic.oup.com/biohorizons/article/doi/10.1093/biohorizons/hzy008/5151366 by DeepDyve user on 10 August 2022 Bioscience Horizons � Volume 11 2018 Research article ............................................................................................... .................................................................. monocultures and mixed cultures in relation to experimental sedi- Westphal, M. I., Browne, M., MacKinnon, K. et al. (2008) The link ment dredging, Aquatic Botany, 95, 61–166. between inter-national trade and the global distribution of invasive alien species, Biological Invasions, 10, 391–398. Strayer, D. L., Lutz, C., Malcom, H. M. et al. (2003) Invertebrate commu- nities associated with a native (Vallisneria americana) and an alien Wilcock, R. J., Nagels, J. W., McBride, G. G. et al. (1998) Characterisation (Trapa natans) macrophyte in a large river, Freshwater Biology, 48, of lowland streams using a single‐station diurnal curve analysis 1938–1949. model with continuous monitoring data for dissolved oxygen and temperature, New Zealand Journal of Marine and Freshwater Tadesse, I., Green, F. B. and Puhakka, J. A. (2004) Seasonal and diurnal Research, 32, 67–79. variations of temperature, pH and dissolved oxygen in advanced integrated wastewater pond system® treating tannery effluent, Wurts, W. A. (1993) Dealing with oxygen depletion in ponds, World Water Research, 38, 645–654. Aquaculture, 24, 108–109. ............................................................................................... ..................................................................

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BioScience HorizonsOxford University Press

Published: Jan 1, 2018

References