Population Ecology of the Endangered Aquatic Carnivorous Macrophyte Aldrovanda Vesiculosa at a Naturalised Site in North America

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Freshwater Biology (2015) doi:10.1111/fwb.12609

Population ecology of the endangered aquatic carnivorous macrophyte Aldrovanda vesiculosa at a naturalised site in North America

† † ‡ § ADAM T. CROSS* , LAURA M. SKATES* , LUBOMΊRADAMEC ,C.MICHAELHAMMOND , § † ¶ PHILIP M. SHERIDAN AND KINGSLEY W. DIXON* *School of Plant Biology, The University of Western Australia, Perth, WA, Australia † Kings Park and Botanic Garden, Perth, WA, Australia ‡ Section of Plant Ecology, Institute of Botany of the Academy of Sciences of the Czech Republic, Trebon, Czech Republic § Meadowview Biological Research Station, Woodford, VA, USA ¶ Curtin University, Perth, WA, Australia

SUMMARY

1. Aldrovanda vesiculosa is an aquatic carnivorous plant native to nutrient impoverished wetland systems in Australia, Africa, Asia, and continental Europe that has declined dramatically throughout its native range in the last century. A strong reliance upon carnivory generally limits its occurrence to specific, nutrient-poor, island-like microhabitats. Remaining native populations are generally small and fragmented, and empirical population ecology data for the species arelacking. Developing an understanding of the constraints to growth, establishment and reproduction in A. vesiculosa is crucial to conservation of the species. 2. In contrast with the decline of the species throughout its native range, a number of large A. vesiculosa populations have become naturalised in North America. This study examines the population ecology of A. vesiculosa at one of these naturalised sites and assesses the species’ potential invasiveness in terms of its ecological characteristics. Transect and quadrat surveys were used to determine the response of morphology, fecundity and spatial distribution to putative biotic and environmental variables, with glasshouse trials and a bird feeding experiment employed to test the persistence of seeds in the seed bank and after transport in bird guts. 3. Although A. vesiculosa is capable of becoming locally abundant (up to 1260 individuals m 2)in wetland areas where biotic and abiotic conditions are optimal, it appears to compete poorly with floating and emergent macrophytes and is limited predominantly to specific microhabitats. The ecological characteristics of A. vesiculosa suggest that it poses a low invasion risk. The species’ growth and reproductive potential are highest in shallow areas harbouring loose vegetation assemblages, with over two thirds of all individuals recorded from water 10–50 cm in depth and in areas with <50% native macrophyte cover. Seeds are unlikely to play a significant role in seasonal persistence or dispersal, with poor floral success (c. 10%), few seeds produced, low seed viability(<50%) throughout the study area and no seeds recovered from the sediment seed bank or recovered from bird faeces following gut transport. 4. The stenotopic ecology of A. vesiculosa, and the continuing decline of dystrophic freshwater wetlands globally, indicate that remaining natural populations are highly sensitive and are likely to decline rapidly without adequate management. In addition to wetland management at the catchment scale to mitigate processes such as eutrophication, future conservation and reintroduction initiatives for A. vesiculosa must focus particularly on the identification, maintenance and restoration of optimal

Correspondence: Adam T. Cross, School of Plant Biology, The University of Western Australia, 35 Stirling Highway, Crawley WA 6009, Perth, Australia; Kings Park and Botanic Garden, Fraser Avenue, West Perth WA 6005, Perth, Australia E-mail: [email protected]

Keywords: carnivorous plant, competition, fecundity, macrophyte, naturalisation, population ecology

methods are predictive trait-based approaches to deter- Introduction mining the invasion risk of particular species (Pheloung, The invasion and naturalisation of exotic species is Williams & Halloy, 1999; Champion & Clayton, 2000; regarded as a major threat to natural ecosystems. The Clayton & Champion, 2006; Pysek & Richardson, 2007; arrival of non-native species, whether through natural Keller & Drake, 2009; Gordon et al., 2012). In addition to dispersal or anthropogenic introduction, often results in providing a crucial tool for the identification, prioritisa- a shift towards new community assemblages and species tion and management of invasive exotic macrophytes, combinations through altered levels of synergism and these studies suggest that a number of introduced spe- trophic interaction (Seastadt, Hobbs & Suding, 2008), cies may pose a comparatively low level of threat to nat- and may significantly impact both biodiversity and eco- ural ecosystems (Ricciardi & Kipp, 2008; Gordon et al., system function (Dıaz et al., 2004). Among weedy plant 2012). These introduced but non-invasive aquatic plants taxa, aquatic macrophytes appear to represent some of possess traits suggesting they are unlikely to signifi- the most pervasive and noxious invaders of natural eco- cantly alter community composition (e.g. poor fecundity, systems (Murphy, 1988; Finlayson et al., 1999; Rejmanek, low dispersive capacity, slow growth rates), or to reduce 2000; Pysek & Richardson, 2007). The effect of these spe- ecosystem function through competitive processes (Lov- cies on ecological function in wetland habitats, as well ell & Stone, 2005). In some instances, it is possible that as the economic costs associated with their control, man- their presence may result in habitation of a previously agement and eradication have been well-studied (Mur- unoccupied ecological niche, rather than influence eco- phy, 1988; Rejmanek, 2000; Anderson, 2003; Lovell & system trajectory towards the development of a hybrid Stone, 2005). The majority of invasive aquatic plants association. share a number of common ecological traits, including a Aldrovanda vesiculosa L. (Droseraceae) is a notable propensity for clonal reproduction, high growth rate, tol- example of an aquatic species given an a priori classifica- erance of a wide range of environmental and climatic tion of ‘non-invasive’ based on an analysis of plant func- conditions, as well as a high vagility and strong propa- tional traits and ecology (Gordon et al., 2012). A gule pressure, often combined with significant disper- submerged, free-floating carnivorous macrophyte native sive capability (Barrett, Eckert & Husband, 1993; to the Old World, A. vesiculosa occurs in nutrient impov- Philbrick & Les, 1996; Santamarıa, 2002; Ricciardi & erished, oligo-mesotrophic and dystrophic (humic) wet- Kipp, 2008; Wittmann et al., 2014). One of the major land systems in Australia, Africa, Asia and continental threats to aquatic ecosystems globally is anthropogenic Europe (Adamec, 1995; Cross, 2012a). The species pos- eutrophication, particularly nitrogen and phosphorus sesses a wide thermal tolerance and an expansive biocli- enrichment from agricultural and urban runoff, and a matic envelope, and was historically distributed across a strong correlation is often apparent between increased significant latitudinal range spanning a number of dif- nutrient loading and the abundance of aquatic weeds in ferent climatic zones. However, it possesses a narrow wetland ecosystems (Carr, Duthie & Taylor,1997; Santa- ecological niche in comparison to other species of similar marıa, 2002; Lacoul & Freedman, 2006; Jennings & Rohr, aquatic affinity and distribution and appears sensitive to 2011; Junk et al., 2013). eutrophication (Kaminski, 1987a; Adamec, 1995; Cross, With a trend towards eutrophication in wetland habi- 2012a). A stenotopic ecology, combined with a strong tats and the environmental impact of aquatic weeds reliance upon carnivory, generally limits the species’ becoming increasingly evident (Finlayson et al., 1999; occurrence within suitable wetlands to specific, nutrient- Amezaga, Santamaria & Green, 2002), predicting inva- poor, island-like microhabitats (Adamec, 1995, 1999, siveness has become one of the major challenges in 2005). Despite exhibiting a degree of tolerance to thermal weed ecology (Rejmanek, 2000; Richardson & Pysek, variation, irradiance and pH (Kaminski, 1987a,b; Ada- 2006). Biodiversity concerns have prompted the develop- mec, 1999), changes in the physico-chemical or biotic ment of mechanistic techniques to assess the invasive- conditions within an inhabited wetland can lead to rapid ness of aquatic plants. Among the most widely utilised local decline (Kaminski, 1987a; Adamec & Lev, 1999;

© 2015 John Wiley & Sons Ltd, Freshwater Biology, doi: 10.1111/fwb.12609 Population ecology of Aldrovanda vesiculosa 3 Adamec, 2005; Cross, 2012a). The majority of terrestrial further elucidate the species’ potential invasiveness in carnivorous plants display specific adaptations to nutri- areas outside its native range. ent-poor conditions (Givnish et al., 1984), and the eutrophication and drying of dystrophic wetland habitats has been implicated as the most significant threat to the via- Methods bility of many aquatic carnivorous plants (Jennings & Site description and population ecology Rohr, 2011). Wetland degradation, primarily through eutrophication, has resulted in a global collapse of A. ve- Meadow Creek is situated in Caroline County, northeast siculosa populations within the last century (Adamec, Virginia, on the east coast of the United States (38°080N, 1995; Cross, 2012a), with the species becoming extinct in 77°240W), and consists of a series of highly humic bea- at least 11 of the 43 countries in which it is known to ver-maintained ponds connected by a braided creek sys- have occurred naturally (a total decline in abundance of tem. Six A. vesiculosa individuals of Japanese origin were around 87%), and unverified status in a further 21 coun- introduced to this site in the late 1990s, and a large pop- tries, prompting listing as Endangered B2ab (iii, v) by ulation has since become naturalised (Cross, 2012a). the International Union for the Conservation of Nature Field surveys were conducted using a canoe in July 2013 (Cross, 2012b). to assess the distribution, abundance, vegetation associa- Despite the species’ increasingly bleak outlook tions and habitat preferences of A. vesiculosa in the Mea- throughout its natural range, populations introduced to dow Creek catchment. Transects were established across several locations in the north-eastern United States dur- the main channel and in surrounding channels, at inter- ing the 1990s appear to have flourished locally (Cross, vals of 60–100 m. The number of A. vesiculosa individu- 2012a; Lamont et al., 2013). This presents a novel situa- als, percent cover of A. vesiculosa, water depth and the tion: the successful naturalisation and local proliferation percent cover of native aquatic macrophytes were of an aquatic carnivorous plant on a continent in which assessed at seven locations using 0.5 9 0.5 m quadrats it has never naturally occurred, completely at odds with at 0.5 m intervals along shore-shore (north-south) tran- the species’ natural Old World populations which dis- sects. Water depth was measured in the southwest cor- play an apparent and increasing trajectory toward ner of each quadrat. Additionally, in two areas where extinction. Previous research has suggested that A. vesic- access by canoe was not possible, 25 quadrats were ran- ulosa is stenotopic, competes poorly with other aquatic domly placed in areas of A. vesiculosa occurrence to sam- plants, and possesses a narrow ecological niche through- ple as previously described. A total of 723 quadrats was out its natural range (Kaminski, 1987a,b; Adamec, 1995, obtained from nine locations. 1999; Adamec & Lev, 1999; Adamec & Kovarova, 2006). However, these studies have generally focused on quan- Population fecundity tifying abiotic site suitability and microhabitat specificity for A. vesiculosa through analysis of the species’ growth Population fecundity was assessed through counts of the rate and morphometrics in response to environmental total number of flowering individuals and the number variation. Empirical data on the population ecology and of fertile fruit and secondary vegetative branches per microhabitat affinity of A. vesiculosa at both local and individual within all sampled quadrats. All fertile fruit regional scales is lacking, and the collection of such data (capsules) were opened to determine the presence and is becoming increasingly difficult as the number of large number of seeds produced. To determine whether A. ve- natural populations continues to dwindle. We examined siculosa was represented in the sediment seed bank, 50 the population ecology of A. vesiculosa at a large natura- samples of the top 2 cm of sediment (5 9 5 cm) were lised site in Virginia, United States, through analysis of collected from Meadowview Pond in areas where the its spatial distribution and morphological characteristics species was most abundant. Sediment was washed and in response to putative biotic and environmental drivers. sieved (250 lm; sensu Ter Heerdt et al., 1996), and exam- Results are presented in the context of the species’ ined carefully under a dissecting microscope to assay for unprecedented global decline, as a comprehensive seeds. The seed testa of A. vesiculosa possesses distinc- understanding of population biology and habitat speci- tive morphological and sculptural characteristics, and on ficity in the species is critical for the successful imple- this basis seeds can be easily distinguished from the mentation of future conservation and restoration seeds of other macrophytes (Cross, 2012a). initiatives. Additionally, data are applied to the weed To examine the capacity of A. vesiculosa seeds to risk assessment classifications of Gordon et al. (2012) to persist in the seed bank, five replicates of 20 freshly

© 2015 John Wiley & Sons Ltd, Freshwater Biology, doi: 10.1111/fwb.12609 4 A. T. Cross et al. collected seeds (collected from cultivated plants) were Peltandra virginica (Location 8); (B) deeper water at the placed into fine nylon mesh bags (250 lm gauge), and fringe of a large, open lake, with Utricularia inflata among buried in the sediment of ex situ A. vesiculosa cultivation Carex festucacea and Peltandra virginica (Location 9); (C) a tanks in Perth, Western Australia, for weekly retrieval shallow swampy area adjacent to the main creek channel, over 12 weeks (n = 1200 seeds). Only filled seeds pos- among Carex alata, Carex lurida, Nuphar advena, Sagittaria sessing an undamaged endosperm and embryo were latifolia, and Typha latifolia (Transect 4); and (D) shallow, used in the experiment, with seed fill determined non- predominantly open water with Utricularia purpurea and destructively by high-resolution X-ray imaging (MX-20 Utricularia inflata among scattered Peltandra virginica, Digital X-ray, Faxitron, Tucson, Arizona, USA). Bags Nuphar advena, and Nymphaea odorata ssp. odorata (Tran- were buried at 1 cm depth at the onset of winter (early sect 1). Four representative quadrats were selected from June), with each attached to a thin plastic stake to facili- transect surveys for each microhabitat, with 25 individu- tate retrieval. Seed fill in retrieved bags was determined als randomly selected from each quadrat. Digital callipers using X-ray imaging, and all filled seeds remaining at were used to measure the length, width, trap size and the the conclusion of the experiment were cut tested to con- internode length of each individual (to the nearest firm viability (Turner et al., 2006). Seeds possessing a 0.1 mm). The total number of living mature whorls, num- firm, white endosperm were deemed to be viable. ber of leaves per whorl and total number of traps for each To provide a preliminary assessment of endozoochor- individual were also recorded, as well as the percentage ous dispersive potential in A. vesiculosa, a bird feeding of traps containing captured invertebrate prey. trial was employed to assess the internal gut transport of seeds. Two pellets each containing 50 A. vesiculosa Water chemistry seeds were force-fed to a captive male Chestnut Teal (Anas castanea; body weight 800 g), using a 15 cm crop An analysis of water chemistry was undertaken to facili- syringe. Five indigestible plastic beads (2 mm diameter) tate a basic comparison of the abiotic conditions between in each pellet acted as markers for seed recovery. The A. vesiculosa microhabitats. The concentrations of NH4- bird had been maintained on a high-fibre manufactured N, NO3-N, total phosphorus, total dissolved organic car- grain-based diet (Layer Crumble, Milne Feeds, Austra- bon and dissolved oxygen as well as values of pH were lia), and pellets were prepared to a similar diameter to determined for 400 mL samples from each of the four ensure they fell within an appropriate food range. The selected microhabitats (Mid-Atlantic Laboratories Inc., bird had last been fed c. 20 h previous to force-feeding. Virginia, USA). These factors are recognised as being After force-feeding, the bird was kept in a small covered among the most significant in determining habitat suit- outdoor enclosure with ample food and water. Time to ability for A. vesiculosa (Kaminski, 1987a,b; Adamec, resume feeding was recorded as an approximate indica- 1995, 1999, 2005; Cross, 2012a). tor of stress. All faeces were collected over the 24 h following force-feeding, with the time of defecation Weed risk assessment recorded and each faeces examined for the presence of A. vesiculosa seeds and plastic marker beads. All recov- Gordon et al. (2012) included A. vesiculosa in a weed risk ered material was examined under high magnification to assessment of 130 aquatic plant taxa in the United States assess its integrity (JCM-5000 Neoscope Scanning Elec- (USAqWRA), in which the risk of invasion for each taxa tron Microscope, Jeol, Netherlands). is determined by the total score from 38 questions. How- ever, several of these questions relate to aspects of biology and population ecology that we empirically address Morphological characteristics for the first time in A. vesiculosa, and thus our results are To assess microsite vigour and the degree to which applied to confirm or revise the USAqWRA predicted growth and development in A. vesiculosa is influenced by invasiveness risk level for the species. The USAqWRA local biotic and abiotic conditions, an assessment of the questions, score guidance, and score for A. vesiculosa are morphological characteristics of 100 individuals from presented in Appendix S1. each of four distinct microhabitats was undertaken. Selected microhabitats are representative of the area’s Data analysis most frequently inhabited by A. vesiculosa throughout the study area, and include: (A) the shallow waters of a Generalised linear models (SPSS Statistics 21, IBM) were braided creek, heavily shaded by dense stands of fitted to determine the main effects of water depth and

© 2015 John Wiley & Sons Ltd, Freshwater Biology, doi: 10.1111/fwb.12609 Population ecology of Aldrovanda vesiculosa 5 percent cover of native macrophytes on the abundance conducted to test the assumptions of normality (Kol- and morphological characteristics of A. vesiculosa (num- mogorov-Smirnov test), linearity, and homoscedasticity ber of total and flowering individuals, percent cover, (Levene’s test). Where necessary, data were log10 trans- plant length and width, mean internode length, trap formed to help meet the assumption of normality and midrib length and the number of apical branches, equal variance. All statistical tests were conducted using whorls and traps per individual; cf. Kaminski, 1987a,b; 95% CI, with significance determined by P < 0.05. Data Adamec, 1999; Adamec & Kovarova, 2006). One-way are presented as mean 1 standard error of the raw ANOVA with Tukey post hoc tests was used to assess data unless stated otherwise. the variation in morphological characteristics within and between each of the seven surveyed areas. Binomial regression models were fitted to A. vesiculosa presence/ Results absence data within R (R Development Core Team, Population ecology 2011) to assess the main effect of water depth and percentage cover of native macrophytes on the species’ Aldrovanda vesiculosa was present in all transects (Fig. 1), occurrence, with a squared term to determine whether with 24,895 individuals recorded from 639 quadrats at the species exhibited an optimum response or a mono- an average density of c. 150 individuals m 2. The species tonic trend. Preliminary analyses of all data were occurred at higher abundance in shallower waters

100 Site 1 80 60 40 20 0 0

–50 cover Percentage –100 Aldrovanda vesiculosa –150 –200 Native macrophytes Water depth (cm) Water depth 100 Site 2 80 60 40 20 0 0

–50 cover Percentage –100 –150 –200 Water depth (cm) Water depth 100 Site 3 80 60 40 20 0 0

–50 cover Percentage –100 –150 –200 Water depth (cm) Water depth 100 Site 4 A 80 60 40 20 0 0

–50 cover Percentage –100 –150 –200 Water depth (cm) Water depth 100 Site 5 80 60 40 20 0 0

–50 cover Percentage –100 –150 –200 Water depth (cm) Water depth 100 Site 6 80 60 40 20 0 0

–50 cover Percentage Fig. 1 Transects across Meadow Creek, –100 –150 Virginia, United States, indicating the –200 Water depth (cm) Water depth percentage cover of Aldrovanda vesiculosa 100 Site 7 80 60 and native macrophytes in relation to 40 water depth. Graph alignment corre- 20 0 0 sponds with relative transect position. –50 cover Percentage –100 Ticks along the X axes indicate 5 metre –150 ater depth (cm) ater depth –200 increments along each transect. W

Table 1 Wetland plant taxa recorded from transects (locations 1–7) and randomised quadrats (locations 8 and 9) in the Meadow Creek catchment, Virginia, United States

Location

Family Species 123456789

Alismataceae Sagittaria latifolia Willd. x Araceae Peltandra virginica(L.) Schott x x x x x x Commelinaceae Commelina virginica L. x Cyperaceae Carex alata Torrey x x x Carex festucacea Schk. ex Willd. x x x x Carex lurida Wahlenb. x x x x x Dulichium arundinaceum (L.) Britton x Droseraceae Aldrovanda vesiculosa L. xxxxxxxxx Eriocaulaceae Eriocaulon decangulare L. x Iridaceae Iris virginica L. x x x Juncaceae Juncus tenuis Willd. x x x x x Lemnaceae Lemna minor L. x Lentibulariaceae Utricularia purpurea Walt. x Utricularia inﬂata Walt. x x x x Utricularia geminiscapa Benj. x x Utricularia macrorhiza Le Conte x x x Nymphaceae Nuphar advena (Ait.) Ait.f. x x x x x x x Nymphaea odorata Aiton ssp. odorata xxxx x x Saururaceae Saururus cernuus L. x Typhaceae Sparganium americanum Nutt. x Typha latifolia L. x

harbouring loose, open vegetation assemblages (up to vegetation (Fig. 1), and a significant negative relation- 1260 individuals per m 2), and generally grew among ship was present between the cover of native macro- floating or emergent wetland plants including Carex luri- phytes and both the number of individuals and da, Peltandra virginica, Nuphar advena, Nymphaea odora- percentage cover of A. vesiculosa (P < 0.001 in both tassp. odorata and Sagittaria latifolia(Table 1). Aldrovanda cases). The majority of A. vesiculosa individuals (c. 75%) vesiculosa co-occurred with native submerged aquatic were recorded from quadrats harbouring <50% native carnivorous plants (Utricularia geminiscapa, U. inflata, macrophyte cover (n = 402), and fewer than 3% were U. purpurea, and U. macrorhiza) in 36 quadrats, predomi- recorded in quadrats possessing >80% native macro- nantly in shallow areas with limited cover (<25%) of phyte cover. No interaction effect was evident between emergent or floating macrophytes. water depth and the cover of native macrophytes on The main effect of increasing water depth was signifi- A. vesiculosa abundance (P = 0.237). Notably, A. vesicul- cant on both the number of individuals and the percent- osa was also absent from the majority (c. 80%) of quad- age cover of A. vesiculosa (P < 0.001 in both cases). A rats in which no native macrophytes were recorded strong optimum relationship was evident between the (n = 108). presence of A. vesiculosa and water depth (P < 0.001), with over two thirds of all individuals (16,787) recorded Population fecundity from water 10–50 cm in depth (n = 371 quadrats). The majority of remaining plants (4,635) were recorded from A marked decline was observed in both the number of depths of between 50 and 100 cm (n = 98), with only flowering A. vesiculosa individuals and the number of around 10% occurring in all remaining quadrats apical branches per individual in response to increasing between 0–10 cm or >100 cm (n = 96). In contrast, a neg- percentage cover of native macrophytes (P = 0.003 and< ative monotonic relationship was evident between 0.001, respectively). The main effect of water depth was increasing water depth and the percentage cover of not significant for either of these factors (P = 0.882 and native macrophytes (P = 0.001). 0.691, respectively). Flower and apical branch produc- The abundance and cover of A. vesiculosa were mark- tion was approximately 50 and 15 times higher, respec- edly reduced in areas of dense emergent or floating tively, in individuals from the shallow, open waters of

Table 2 Morphological characteristics and population ecology of Aldrovanda vesiculosa from four different microsites in the Meadow Creek catchment, Virginia, United States. A: In the shallow water of a braided creek, heavily shaded by dense stands of Peltandra virginica(Location 8); B: In deeper water at the fringe of a large, open lake, growing with Utricularia inflata among Carex festucacea and Peltandra virginica (Loca- tion 9); C: In a shallow swampy area adjacent to the main creek channel, among Carex alata, Carex lurida, Nuphar advena, Sagittaria latifolia and Typha latifolia (Transect 4); D: In shallow, predominantly open water with Utricularia purpurea and Utricularia inflata among scattered Peltandra virginica, Nuphar advena, and Nymphaea odorata ssp. odorata (Transect 1). Data are presented as mean one standard error where possible, with four quadrats and 100 individuals assessed for each location. Annotated lettering indicates statistical significance between locations for each parameter (P < 0.05)

Microhabitat

AB C D

Microhabitat characteristics Native macrophyte cover (%) 90.7 1.2a 69.5 6.3b 43.2 4.1c 5.3 9.2d Aldrovanda vesiculosa cover (%) 23.7 4.1a 5.0 2.2b 56.5 11.6c 83.1 9.0d Depth (cm) 23.6 3.1 47.3 0.7 34.1 5.0 26.5 0.5 Water chemistry 1 NH4-N (mg L ) 0.12 0.08 0.10 0.08 1 NO3-N (mg L ) 0.32 0.23 0.25 0.24 Total phosphorus (mg L 1) 0.26 0.16 0.49 0.18 Dissolved oxygen (mg L 1) 8.59 9.52 8.25 9.14 Total organic carbon (mg L 1) 10 7.6 7.8 7.2 pH 5.81 6.27 5.72 5.70 Aldrovanda vesiculosa individuals Length (mm) 64.3 3.8a 101.1 7.3b 122.7 5.6c 147.1 4.0d Width (mm) 11.9 0.4a 12.4 0.3a 16.2 0.2b 18.6 0.2c Number of apical branches 0.2 0.1a 1.3 0.2b 2.2 0.5c 3.0 0.4c Percentage of individuals in ﬂower 0.1 0.1a 0.1 0.1a 2.2 0.2b 4.9 0.5c Leaves per whorl 6.8 0.1a 7.0 0.1a 7.3 0.1b 7.5 0.1b Number of whorls 16.1 0.7a 20.9 0.6b 22.3 0.6c 28.5 0.3d Internode length (mm) 4.0 0.1a 5.0 0.1b 5.4 0.1c 5.2 0.1c Trap size (mm) 1.9 0.1a 2.0 0.1a 4.6 0.1b 5.6 0.1c Total number of traps 102.8 7.3a 121.4 5.0b 163.8 5.1c 212.1 3.0d Whorls with prey per individual (%) 15.7 2.4a 20.2 4.7b 25.1 4.3c 36.5 8.7d

Location 1 than in the heavily vegetated Location 8 after 3 and 6 months of burial in ex situ cultivation (Table 2). Flowering success throughout the study site tanks, respectively. All seeds remaining at the end of the appeared poor, with only 98 fertile fruit recorded experiment were determined to be viable. The majority (c. 10% of flowers recorded). However, the majority of of non-viable seeds appeared rotten or had suffered fun- fertile fruit were collected from Transect 1 (42), Transect gal attack, and exhibited a black, spongy endosperm 2 (18), and Transect 4 (14). Seed set was low, ranging containing fungal hyphae. from one to nine seeds per fruit (mean 5.7 0.9), and No intact seeds were recovered from bird faeces dur- did not vary significantly between transects (P = 0.633). ing experimental feeding trials, and no seeds were Seed fill was also relatively low (45.2 6.4%). recovered from food or water bowls to indicate regurgi- No A. vesiculosa seeds were recovered from sediment tation within the 24 h period. Several large A. vesiculosa samples. Sediment seed bank assays yielded 143 seeds seed coat fragments (0.2–0.3 mm) were recovered at of at least 10 species, predominantly Carex lurida (72 90 min, followed by numerous minute fragments seeds), C. aquatilis (66), Nymphaea odorata ssp. odorata (<0.1 mm) recovered between 3–8 h. A single intact (42), C. festucacea (22) and C. alata (20). Seeds of addi- Cyperaceae seed was recovered after 30 min, possibly tional species retrieved included Nuphar advena (8), Pelt- originating from the Scirpussp. surrounding the enclo- andra virginica (6), Commelina virginica (4), Iris virginica sure. All plastic markers were recovered intact after 8 h. (2) and Eriocaulon decangulare(1). Thirty-six retrieved seeds could not be identified. Morphological characteristics The viability of A. vesiculosa seeds in experimental sediment persistence trials (as indicated by seed fill) All measured morphological characteristics varied sig- declined rapidly from 100% to 65 5% and 38 4% nificantly between transects (P < 0.05), with Transect 1

© 2015 John Wiley & Sons Ltd, Freshwater Biology, doi: 10.1111/fwb.12609 8 A. T. Cross et al. harbouring the largest and most vigorous individuals limited. Most significantly, although sexual reproduction (Table 2). In addition to exhibiting markedly increased was limited across the entire study site, the number of average length and width, plants at Transect 1 possessed flowering individuals in these locations was up to 50 the highest average number of whorls, leaves per whorl, times higher than in deeper or heavily vegetated micro- trap size and number of traps per individual. A signifi- habitats. A high rate of apical branching is indicative of cant negative monotonic relationship was evident the suitability of growing conditions for A. vesiculosa between the length, width, number of whorls, trap size (Kaminski, 1987a; Adamec, 1999), and the highest rates and total number of traps per individual in response to of apical branching were observed in areas where com- increasing cover of native macrophytes (P < 0.01 in all petition was limited. Previous studies have suggested cases). No relationship was evident between measured that optimal irradiance for A. vesiculosa growth is morphological characteristics and water depth. around 3050% of incident sunlight, with the species’ growth significantly reduced in more heavily shaded conditions (Adamec, 1997, 1999; Adamec & Kovarova, Water chemistry 2006). As the production of flowers and apical branches Water chemistry analysis indicated that all four sampled was not responsive to water depth, it would appear that microsites were probably dystrophic (sensu Smith, Til- competition is one of the most significant constraints on man & Nekola, 1999), and display nutrient concentra- reproductive success in A. vesiculosa. tions indicating that they are likely to be meso-eutrophic Although A. vesiculosa was present throughout the (Table 2). Waters were acidic, rich in organic carbon and study site in areas of different water depth and in vari- contained moderate-low concentrations of NH4-N, NO3- ous vegetation assemblages, results from this study sup- N and total P. port the previously reported propensity of A. vesiculosa to favour shallow dystrophic waters harbouring loose, open assemblages of emergent and floating macrophytes Weed risk assessment (sensu Kaminski, 1987a; Adamec, 1999; Adamec & Lev, A revision of the predicted invasiveness risk level for 1999). All measured morphological characters were A. vesiculosa against the USAqWRA criteria resulted in a greatest in the shallow and predominantly open waters score of 29 (Appendix S1). This suggests the species pos- of Transect 1, where A. vesiculosa grew with native sub- sesses a low invasiveness risk level (determined by a merged aquatic carnivorous plants (Utricularia purpurea threshold score of 31), and supports the existing a priori and U. inflata) among scattered Peltandra virginica, Nu- classification of A. vesiculosa as a ‘non-invader’. phar advena, and Nymphaea odoratassp. odorata. Aldrovanda vesiculosa was rarely present at high percentage cover (>70%) in areas of deep water or high native macrophyte Discussion cover, with the exception of several slowly flowing dee- Here, we present the first large-scale analysis of popula- per areas (5080 cm) where the species grew in open tion ecology for the globally endangered Aldrovanda water among the floating leaves of Nymphaea odoratassp. vesiculosa and provide the first evidence of a link odorata. Water depth has been previously reported as a between fecundity and microhabitat in this species. significant determinant of habitat suitability in A. vesicul- Results indicate that the growth and fecundity of A. ve- osa (Adamec, 1999; Adamec & Lev, 1999). In this study, siculosa are highly responsive to both biotic and abiotic the species exhibited an optimum response to water habitat factors and that the species possesses a limited depth, and was consistently recorded from shallow capacity to compete with native North American aquatic water (1050 cm deep). Although shallower habitats plants. The most significant factors influencing growth (<10 cm) may exhibit suitable water chemistry condi- and fecundity included water depth and competition tions, studies suggest that these areas may be more from emergent and floating macrophytes, with water prone to water level fluctuations and encroachment from chemistry and the abundance of invertebrate prey also emergent macrophytes or terrestrial plants (Adamec, likely to play a significant role in determining microhab- 1999, 2005). itat suitability. A strong increase in plant performance High competition also appears to limit the abundance was evident along a habitat suitability gradient, with the and growth of A. vesiculosa, with both the size and num- highest average values for all measured morphological ber of individuals decreasing with a corresponding and reproductive characters recorded from shallow increase in the percentage cover of native macrophytes. areas where competition from native macrophytes was The pooled cover of native macrophytes displayed a

© 2015 John Wiley & Sons Ltd, Freshwater Biology, doi: 10.1111/fwb.12609 Population ecology of Aldrovanda vesiculosa 9 contrasting trend in response to water depth, and the lake in 2003 appears to have been from seeds (L. Ada- effect of water depth on A. vesiculosa abundance was mec, unpubl. data), suggesting that seed bank develop- independent of the effect of native macrophyte cover. ment may be variable between populations or The poor performance of A. vesiculosa in heavily vege- dependent upon as yet unknown environmental factors. tated areas is likely to result from limited irradiance at The dispersive capacity of A. vesiculosa warrants fur- water level, reduced surface water temperature and ther research. In order for propagules to disperse and altered water chemistry (particularly pH and reduced establish at new locations, they must possess the capac- CO2 concentration); all these are regarded as critical ity to survive dispersal conditions (Santamarıa, 2002). parameters in the species’ optimum growth (Kaminski, For endozoochorous (internal) transport by waterbirds, 1987a,b; Adamec, 1997, 1999; Cross, 2012a). However, this implies a capacity to withstand the chemical and dense strands of floating and emergent taxa are also mechanical processes within the avian gut for a suitable likely to provide physical obstruction, limiting both the period of time (Claussen et al., 2002; Figuerola & Green, clonal growth of A. vesiculosa and its local dispersal by 2002; Santamarıa, 2002). Vegetative tissue in A. vesiculosa wind or water movement. A high concentration of CO2 is thin and easily fragmented, and thus it would appear in particular is regarded as crucial for optimal growth in unlikely that vegetative propagules (e.g. stem fragments A. vesiculosa, and is generally associated with shallow and turions) possess this capacity (see Claussen et al., acidic waters with deep organic sediments (Adamec, 2002). Preliminary evidence from this study suggests 1997, 1999, 2005). However, it is also likely that the pro- that seeds also do not survive internal bird gut trans- pensity for A. vesiculosa to occur in shallow areas may port, with all seeds entirely or partially digested. be a result of reduced water currents in these habitats, a Although our experiment was not replicated due to the factor likely to be important for rootless submerged availability of only a single Anascastanea individual, pre- aquatic plants. Field growth trials indicate that prey cap- vious studies have also drawn conclusions regarding the ture and a degree of eutrophication significantly increase digestibility of aquatic plant seeds from only a single growth rate in A. vesiculosa, with significantly higher experimental bird (Smits, Van Ruremonde & Van Der growth rates observed at a meso-eutrophic site with Velde, 1989; Camenisch & Cook, 1996). It would appear high prey availability than at an oligo-mesotrophic site likely, based on the available evidence, that dispersal in with low prey availability (Adamec & Kovarova, 2006). A. vesiculosa, at least at local scales, is facilitated by The strong correlation between growth and flowering either hydrochory or exozoochory. Anecdotal evidence with prey capture in this study in microsites with simi- suggests that the movement of beavers may have facili- lar nutrient status suggests that higher rates of prey cap- tated the upstream spread of A. vesiculosa in Meadow ture are beneficial for both development and fecundity Creek, with downstream dispersal occurring predomi- in A. vesiculosa. nantly during flood events following winter ice melt, Clonal aquatic plants with extensive lateral spread and individuals blown by wind into shallow littoral exhibit some of the lowest rates of sexual reproductive areas (sensu Adamec, 1995; Adamec & Lev, 1999). Ada- output (Herben, Sera & Klimesova, 2014), and it is per- mec (1999) observed ducks grazing on free-floating haps unsurprising therefore that the production of flow- A. vesiculosa turions at naturalised locations in Europe, ers and successful seed set in A. vesiculosa were low and suggested that, in addition to waterbirds, the move- across the entire study site. Similarly, low levels of floral ment of larger animals such as deer in the littoral zone success and seed set have been previously reported for may also spread vegetative propagules. The deliberate the species (Nakano, 1992; Adamec & Tichy, 1997; Ada- or accidental movement of A. vesiculosa plants or frag- mec, 1999; Cross, 2012a). No A. vesiculosa seeds were ments by anthropogenic means (particularly through recovered from the sediment seed bank. A seed survival recreational activities such as boating) is also plausible. rate of less than 40% after 6 months under experimental However, empirical evidence to implicate any particular conditions suggests that very few seeds are likely to per- dispersive mechanism in the movement of A. vesiculosa sist in the sediment seed bank between seasons. This between suitable habitats is lacking. low survival rate, combined with the limited seed set Population ecology data from this study, combined and a low seed viability observed, indicates that sexual with the results of previously published studies of ecol- reproduction is unlikely to play a major role in the inter- ogy and biology in A. vesiculosa (e.g. Adamec & Lev, seasonal persistence of A. vesiculosa at the study site. 1999), suggest that the species possesses a low invasive- However, the recovery of a native A. vesiculosa popula- ness risk level and support the existing a priori classification at Lake Balata-t o, Hungary, following drying of the tion of A. vesiculosa as a ‘non-invader’ (Gordon et al.,

© 2015 John Wiley & Sons Ltd, Freshwater Biology, doi: 10.1111/fwb.12609 10 A. T. Cross et al. 2012). Although the species is a rapidly growing clonal In the face of continuing decline of A. vesiculosa submerged macrophyte and therefore possesses the throughout its natural range, management initiatives capacity to proliferate quickly in areas of suitable habitat should focus on the conservation of suitable habitat and (Adamec, 1999), the species’ ability to attain optimal the repatriation of populations into rehabilitated areas. growth appears significantly constrained by its steno- In particular, focus should be placed on the determina- topic ecology to small microhabitats (tens to hundreds tion and ongoing management of specific microhabitats of m2; Adamec, 2005). Our study did not assess species- that provide optimal conditions for the species’ growth specific competitive interactions, and we acknowledge and reproduction. Data from this study support previ- that the pooling of native macrophytes into a single vari- ous conclusions that A. vesiculosa possesses little capacity able may overlook the occupation of different niches by to become invasive (e.g. Adamec & Lev, 1999), and does these taxa along the water depth gradient. However, all not appear to compete significantly with other aquatic measured growth parameters for A. vesiculosa displayed macrophytes. However, further research is required to significant responsiveness to biotic and abiotic factors, elucidate the potentially cryptic impacts of A. vesiculosa and data provided no evidence to suggest A. vesiculosa on ecosystem functioning, in particular its effect on local poses a competitive threat to native aquatic plants. Car- invertebrate communities. If these impacts prove to be nivorous macrophytes from the genus Utricularia are minor, carefully managed assisted dispersal in some perhaps the most likely group to be affected by the nat- regions may represent a viable conservation tool given uralisation of A. vesiculosa in any given habitat, given the apparent lack of genetic variation present between the similar reliance of these taxa on carnivory for sur- A. vesiculosa populations globally (Maldonado San Mar- vival. However, these taxa are commonly found growing tin et al., 2003; Elansary, Adamec & Storchova, 2010). sympatrically throughout the natural range of A. vesicul- Introductions at a number of locations where A. vesiculosa (Kaminski, 1987a; Adamec, 1995; Vilkonis, 2004; Cross, osa historically did not occur in Europe appear to have 2012a), and the frequent co-occurrence of A. vesiculosa resulted in stable, persistent populations (Adamec & with Utricularia geminiscapa, U. inflata, U. purpurea and Lev, 1999; Adamec, 2005; Cross, 2012a), and may offer U. macrorhiza in the study area suggests that the two gen- places of refuge to a species which otherwise appears to era may occupy slightly different niches within a common be on a trajectory towards extinction. microhabitat. No negative effects on native aquatic Utricu- laria or other aquatic plants have been documented Acknowledgments 10 years after naturalisation of A. vesiculosa in the Czech Republic (e.g. Adamec & Lev, 1999; Adamec, 2005), and The authors thank the Chase family for providing access experimental and field trials suggest that A. vesiculosa and to Dalton Millpond, and the Horton family for providing aquatic Utricularia may possess different growth strate- access to areas of Meadow Creek. Helpful comments on gies and prey selectivity (Adamec & Kovarova, 2006; Ada- the manuscript from Dr David Merritt and Dr Shane mec, Sirova & Vrba, 2010). Future studies should examine Turner were greatly appreciated. Critical review of the the potential competitive relationships between A. vesicul- manuscript by Professor Roger Jones and two anony- osa and Utricularia in greater detail. mous reviewers is gratefully acknowledged. This work While A. vesiculosa does not appear to represent a com- was supported by an Australian Postgraduate Award to petitive threat to native aquatic plants, the species’ impact ATC from the Commonwealth of Australia and by a on native aquatic invertebrate communities may be signif- long-term research project from the Czech Academy of icant. With up to c. 40% of traps containing captured prey Sciences No. RVO 67985939 to LA. in suitable microhabitats, and approximately 200 traps per individual in these areas, it is evident that large num- References bers of invertebrates are captured. Although A. vesiculosa Adamec L. (1995) Ecological requirements and recent has been reported to preferentially capture mosquito lar- European distribution of the aquatic carnivorous plant vae (Cross, 2012a), and may therefore be beneficial in con- Aldrovanda vesiculosa L.- a review. 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