Science of the Total Environment 517 (2015) 222–231

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Black spots for aquatic and terrestrial ecosystems: impact of a perennial cormorant colony on the environment Piotr Klimaszyk a,⁎, Andrzej Brzeg b, Piotr Rzymski c, Ryszard Piotrowicz a a b c

Department of Water Protection, Adam Mickiewicz University, Umultowska 89, 61-614 Poznań, Poland Department of Plant Ecology and Environment Protection, Adam Mickiewicz University, Umultowska 89, 61-614 Poznań, Poland Department of Biology and Environmental Protection, Poznan University of Medical Sciences, Rokietnicka 8, 60-806 Poznań, Poland

H I G H L I G H T S

G R A P H I C A L

A B S T R A C T

• The complexity of ecological effects of cormorants colonies were investigated. • Soil chemistry and plant vegetation were altered via extreme nutrients deposition. • Promotion of nitrophilous and invasive alien species was observed. • Large loads of nutrients were transferred to nearby lake through surface runoff. • The colony increased coliform numbers in the nearby littoral zone.

a r t i c l e

i n f o

Article history: Received 12 November 2014 Received in revised form 18 February 2015 Accepted 19 February 2015 Available online 27 February 2015 Editor: F. Riget Keywords: Cormorants Surface runoff Soils Nitrogen Phosphorus Plant vegetation

⁎ Corresponding author. E-mail address: [email protected] (P. Klimaszyk).

http://dx.doi.org/10.1016/j.scitotenv.2015.02.067 0048-9697/© 2015 Elsevier B.V. All rights reserved.

a b s t r a c t The global growth of populations of different cormorant species has raised concern on the consequences of their presence in the environment. This study examined the impact of a perennial colony (160 breeding pairs) of great cormorants on terrestrial and aquatic ecosystems. The deposition of bird-originating nutrients within the area of colony, their accumulation in soils and the fluxed of chemical substances to a nearby lake were investigated. The impact of cormorants on terrestrial vegetation and microbial pollution of the lake were also studied. The soils beneath the colony were found to contain extremely high concentrations of nitrogen and phosphorus. The overgrowing vegetation was largely limited with nitrophilous and invasive species being more abundant. Increased loads of organic matter, nitrogen and phosphorus were also found in groundwater and particularly, surface runoff. The colony area delivered significant amounts of nutrients to the lake also when the birds were absent. The lake water near colony was also characterized by increased nutrient content and additionally higher number of faecal bacteria. The present results demonstrate the complexity through which the effect of cormorant colonies can be manifested simultaneously in terrestrial and aquatic ecosystem. © 2015 Elsevier B.V. All rights reserved.

P. Klimaszyk et al. / Science of the Total Environment 517 (2015) 222–231

1. Introduction Cormorants (Phalacrocorax), large piscivorous birds, demonstrate a nearly global distribution encompassing Asia, Africa, Australia and New Zealand, North America and Europe (Kennedy and Spencer, 2014). Considered by humankind as the competitors for fish resources, they were largely exterminated and their number remained low over the decades (Ostman et al., 2013). However, over the past 40 years, a great rise in the population of some species such as the North American double-crested cormorant (Phalacrocorax auritus Less.) and the great cormorant (Phalacrocorax carbo L.) has been observed (van Eerden and Gregersen, 1995; Bzoma et al., 2003; White et al., 2011; Rusell et al., 2012; van Eerden et al., 2012). Several reasons appear to be responsible for this phenomenon among which are: the decision to protect these birds in numerous countries, their high degree of ecological adaptation, ability to forage on marine and freshwater ecosystems, increase in fish biomass due to the eutrophication of surface waters and global climate changes (White et al., 2011; Skov, 2011). Changes in the population status of cormorants have raised serious concerns as to the consequences of their presence in the environment. In many cases these birds can colonize forested areas located directly adjacent to water bodies and therefore potentially affect the functioning of both the terrestrial and aquatic ecosystem (Klimaszyk et al., 2015). Piscivorous birds such as cormorants represent a very important intermediate link in some food webs (Gwiazda et al., 2014; Skov et al., 2014) and a factor facilitating the dislocation of matter between aquatic and terrestrial ecosystems (Marion et al., 1994; Huang et al., 2014). Their diet is rich in nitrogen (N) and phosphorus (P), which results in a significantly higher excretion of these elements than in herbivorous birds (Marion et al., 1994; Sterner and Elser, 2002). During the breeding season, cormorants feeding on fish can deposit a large amount of biomass and chemical compounds beneath the colony area (Kameda et al., 2006). This usually results in a relevant increase in the status of N and P in soil (Mulder and Keall, 2001), a factor that has a great influence on primary production in terrestrial environments (Vitousek and Howarth, 1991). On the other hand, some studies have indicated that piscivorous birds can successfully prevent the eutrophication of lakes due to the exclusion of N and P from the aquatic food chains and their consequent introduction to terrestrial biochemical cycles (Ligęza and Smal, 2003). Moreover, the foraging of cormorants can lead to the top-down control of the aquatic food web. This has been observed particularly in the case of small lakes, in which a significant decrease in the number of fish led to simultaneous increase in zooplankton density followed by the limited development of phytoplankton (Gmitrzuk, 2004). It is, however, worth noting that cormorants inhabiting one colony can feed on a relatively large area (up to 30 km from the colony) and on various water systems. At the same time, most of their excrements are deposited over a small area under the colony (Marion et al., 1994; Kameda et al., 2006) and near the lake shore (Klimaszyk et al., 2015). As the high deposition of nutrient-rich faeces of cormorants successfully limits terrestrial vegetation (Ellis et al., 2006), the large loads of chemical compounds can be transported with surface runoff or groundwater to the nearby lake (McCann et al., 1997; Klimaszyk et al., 2014). In such cases, cormorants can increase the bioavailable pool of N and P, promote primary production and trigger the eutrophication of surface waters (McCann et al., 2000; Klimaszyk et al., 2015). Altogether, the effect of cormorants on the inhabited environment is most likely complex and its assessment requires multifaceted investigations. The present study evaluated the degree to which a perennial colony of the great cormorant affects terrestrial and lake ecosystems. The following hypotheses have been put forward: (i) The deposition of nutrients originating from cormorant feaces significantly alters soil chemistry and induces long-term changes in plant communities. Plant species characteristic for forest

223

are replaced by nitrophilous and alien species, and biodiversity decrease. (ii) The cormorant-induced havoc in terrestrial vegetation promotes the surface runoff — overland flow is a main route of nutrients transfer from colony to aquatic environment. (iii) The cormorant-derived N and P can constitute a significant share in nutrient budget of the surface freshwaters and promote their eutrophication. To verify these hypotheses the chemistry of soil beneath the cormorant colony, out-flowing groundwater and surface runoff, and nearby lake as well as microbial pollution of the littoral and differences in the terrestrial vegetation were investigated. Our study clearly demonstrates the complexity through which the effect of cormorant colonies can be manifested simultaneously in terrestrial and aquatic ecosystem. 2. Material and methods 2.1. Study site — lake The study area covered the cormorant (P. carbo) colony located on the island shore of Lake Ostrowiec (Northern Poland, Europe) at the latitude and longitude of 53°4′39″N and 15°57′66″E, respectively (Fig. 1). The lake consists of four basins. Exchange of water between them is hampered due to shallow isthmuses. The River Plociczna flows into and out of the northern basin of the lake, and this basin can be described as a through-flow basin, in contrast to the other lake basins, with no outflow (Klimaszyk et al., 2014). The total area of the lake is almost 400 ha and shoreline length is over 22 km. The maximum depth of the lake is 27.9 m. The immediate-direct catchment area of Lake Ostrowiec covers about 10 km2, while the area drained by the River Płociczna is almost 202 km2. More than 90% of the direct catchment area is covered by forest — over 70 year old plantations of Scots pine (Pinus sylvestris). Three islands with areas ranging from 2.2 to 0.6 ha are located on the lake (Fig. 1). The islands are overgrown by climax forest with the domination of: sessile oak (Quercus petrea), European beech (Fagus sylvatica) and Scots pine (P. sylvestris). 2.2. Study site — cormorant colony Great cormorants have been observed on Lech Island (1.2 ha) at Lake Ostrowiec since the late 1960's. Until the early 1990's the number of breeding pairs did not exceed 50. From 1995 the number of birds started to increase. In 2004 almost 300 inhabited nests were reported and due to the withering of trees, the colony expanded from the central part of the island to an area closer to its edge. During the investigation period (March 2010–March 2012) the number of cormorants varied from 154–167 breeding pairs. At that time the birds did not occupy the central part of the island (site A; 0.39 ha; hereafter former colony) due to the lack of trees. The main colony (nearly 90% of nests) was located in the surrounding area (site B; 0.38 ha; hereafter central colony) where most of the trees were already withered. The peripheral zone of the island (site C; 0.43 ha; hereafter peripheral colony) was rich in vegetation and the number of nests did not exceed 20 (Fig. 1). 2.3. Sampling Samples of cormorant droppings were collected monthly (at the beginning of the month) from April to October 2010 using 10 trays (60 × 60 cm) distributed for 24 h in transects (Fig. 1). Plant detritus (leaves, branches) found in trays was removed and not taken into consideration. The deposition of nutrients was recalculated as a monthly load of N and P per m2. During sample collection, the number of adult cormorants inhabiting the colony was counted.

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Fig. 1. Study site (Lake Ostrowiec) and location of the sampling sites.

Samples of soil were collected bimonthly between March 2010– March 2012 from the peripheral, central and former colony area. As a control, samples were also collected from the other island on Lake Ostrowiec on which no cormorant colony has ever existed. Samples were collected at 3 genetic soil horizons: organic — the ectohumic soil horizon at a depth of 0–5 cm, the eluvial horizon at a depth of 5–25 cm, and the mineral horizon at a depth of N25 cm. Collected soil samples were air-dried and sieved using a 1 mm sieve to separate gravel (particle size N1 mm) and non-soil components and stored in a freezer at −20 °C prior to analyses. Samples of surface runoff were collected using PVC gutter samplers (3 m long and 0.15 wide) with sealed plastic collectors buried at the lower end at an angle that prevented the direct inflow of rainwater (Klimaszyk and Rzymski, 2013a). Gutters were placed under the forest litter and covered with a 0.25 mm mesh. Care was taken to ensure minimal soil disturbance in the installation of the gutters. Two samplers were installed on the slopes within the peripheral colony (Fig. 1) and two others at corresponding slopes on the control island not inhabited by these birds. All sites, studied and control, were characterized by a significant inclination (45° beneath the colony and 40° at the control), exposed to the north-west and close to the edge of the island. Runoff water was collected between March 2010–March 2012 after each precipitation event and during melting of the snowpack.

Samples of shallow groundwater were collected bimonthly (between March 2010–March 2012) from piezometers — wells installed near the surface runoff samplers. To remove soil particles, collected samples were filtered through a cellulose filter GF-C. Samples for DOC analysis were filtered through a cellulose nitrate filter — pore size 0.45 μm. Surface lake water was collected in transect (littoral area near the colony, 50 m from the colony, 100 m from the colony and the central part of the lake). Samples of lake water collected for microbial analyses were stored in sterile vessels. Following the collection, samples of runoff, groundwater and lake water were transported to the laboratory in a lightproof insulated box containing a cooling factor. Usually the laboratory analyses were conducted immediately after transportation, if not, samples were frozen at −20 °C. 2.4. Surface runoff, groundwater and water lake analyses Electric conductivity and pH of water were measured in the field using a YSI 556 Multiparameter Instrument. In the laboratory the following parameters were analysed: ammonium nitrogen (N-NH4, using the Nessler method), nitrites (N-NO2, using the sulphanic acid method), nitrates (N-NO3, using the sodium salicylate method), organic nitrogen (Norg., using the Kjeldahl method), total phosphorus (TP, using

P. Klimaszyk et al. / Science of the Total Environment 517 (2015) 222–231

225

Fig. 2. Mean (±SD) deposition of TN (A) and TP (B) at cormorant colony in relation to the number of birds.

the molybdate method after mineralization) and orthophosphates (TRP, using the molybdate method) (APHA, 2005). Dissolved organic carbon (DOC) was measured using a SHIMADZU TOC-5000 A analyzer. 2.5. Soil analyses The total amount of nitrogen (NtK) in soils was determined using the Kjeldahl method (van Reeuwijk, 2002), constituting the sum of Norg and N-NH4. Contents of N-NO3 and N-NH4 were determined after extraction in CH3COOH (0.03 mol L−1) using the Nessler method, while N-NO2 was analysed using a method with phenoldisulphonic acid (Prince, 1955). TP content in soils was determined at 850 nm using a Shimadzu UV1610 spectrophotometer (molybdate method) after burning the samples at 550 °C and mineralizing in suprapure HNO3 (14 mol L−1) and H2SO4 (18 mol L−1) (Sobczyński and Joniak, 2009).

2.8. Calculations and statistical analyses The results were analysed with Statistica 10.0 software (StatSoft, USA). Gaussian distribution was tested with Shapiro–Wilk's test. Data that did not meet this assumption were analysed using the nonparametric Mann Whitney U test (water samples) and Wilcoxon test (soil samples from different horizons). Normally distributed data were compared using the T-Student test. A p value of b0.05 was considered as statistically significant. The data from the period between April and September were representative for the breeding season; the rest of the year was treated as an off-season. 3. Results 3.1. Impact on nutrient supply at colony area

2.6. Microbiological analyses The number of coliform bacteria and Escherichia coli in lake water was measured using IDEXX Colilert®-18 (ISO 9308-2:2012). The samples were incubated in trays (Quanti-Tray®/2000, IDEXX) for 20 ± 2 h at 37 °C, after which yellow wells were counted and the most probable number (MPN) for coliform bacteria was determined. Under UV light, fluorescing wells were counted and used to determine the MPN of E. coli in the samples.

The annual nutrient flux from cormorant droppings to the inhabited area was estimated at 14 g m−2 for N and nearly 8.5 g m−2 for P. Total annual N and P load delivered by the birds rose to 184 kg and 131 kg, respectively. The highest mean supply of nutrients, 6 g m−2 per month for N and over 4 g m−2 for P, was observed during the greatest abundance of cormorants (Fig. 2). Nutrients were deposited unevenly within the colony area. The highest loads of faeces were deposited directly beneath the central part of colony while the lowest load was found at the peripheral colony zone and former colony (Fig. 2).

2.7. Terrestrial vegetation analyses 3.2. Impact on soil chemistry The identification of the vegetation covering the slopes beneath the cormorant colony and at the control island was carried out in July 2011. Plant species were analysed in transect with a width of 15 m, perpendicular to the shoreline and traversing the island from the top to the edge (Fig. 1). Plant communities and density of individual species were effected in accordance with generally accepted principles of geobotanical charting, noting coverage of the bed area by individual species within each determined phytocoenoses. Abundance range was expressed in the Braun-Blanquet scale (Braun-Blanquet, 1964).

The cormorant colony had a significant effect on soil chemistry — extremely high concentrations of N and P were noted. The greatest loads of these elements were accumulated in the surface layer of the central colony (with the highest number of nests). Nevertheless, the concentrations found at the peripheral and former colony were still at least several-fold higher than those in the soil of the control (Table 1). The N pool at colony sites was dominated by Norg ranging from 635.6 to 1794.2 mg kg− 1. The concentrations of TP were also extremely high

Table. 1 Content of nutrients in soils (±SD) under cormorant colony (A — central part of the colony; B — former colony area; C — peripheral colony) and control (D), and the statistical significance of differences between colony and control sites (A, D n = 18; B, C n = 6). N-NH4 [mg kg−1]

N-NO3 [mg kg−1]

Norg [mg kg−1]

TP [mg kg−1]

Layer

A

B

C

D

A

B

C

D

A

B

D

A

Organic

211.6

763.8 ±

425.1

30.1 ±

56.2

346.3 ±

189.2

6.82 ±

635.6

1794.2 ± 1310 ±

311.3 ±

3175.5 ± 3951.2

1521.2 ± 66.2 ±

277.9 165.7 ±

± 59.8 78.9 ±

1.8 23.9 ±

± 6.1 51.2

108.8 183.2 ±

± 39.9 41.6 ±

1.09 4.95 ±

± 156 258.8

424.6 593.2 ±

780.5 585.3 ±

41.21 187.2 ±

202.2 522.2 ±

± 1328 317.7 ±

102.2 167.3 ±

6.52 58.2 ±

35.1 73.5 ±

11.2 32.6 ±

1.11 22.7 ±

± 6.6 40.6

31.35 50.5 ±

3.1 36.6 ±

0.61 4.5 ±

± 55.2 133.2

194.1 370.2 ±

72.7 201.5 ±

15.62 33.3 ±

89.1 262.5 ±

57.3 179.2 ±

25.1 78.9 ±

11.69 38.4 ±

3.6

0.98

± 4.1 4.81 p b 0.001 for all

3.1

0.33

± 25.1 39 p b 0.001 for all

36.2

2.69

19.3 38.8 p b 0.001 for all

8.1

4.94

± 29.6 Minero66.2 ± organic 7.1 Mineral 55.8 ±

5.1 6.29 Wilcoxon p b 0.001 for all test

C

B

C

D

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Table 2 Occurrence and abundance range of plant species at cormorant colony (A — central part of the colony; B — former colony area; C — peripheral colony) and control site. Colony A Trees Tilia cordata a Quercus petraea a Quercus petraea c Pinus sylvestris a Alnus glutinosa a Betula pendula a Fraxinus excelsior a/c Fagus sylvatica a Fagus sylvatica b Fagus sylvatica c Sorbus aucuparia c Shrubs Sambucus nigra b Sambucus nigra c Rosa canina b Cornus sanguinea b Euonymus europaea b Frangula alnus b Frangula alnus c Rosa sherardii b Juniperus communis b Herbs Poa nemoralis Calamagrostis epigejos Rubus idaeus Melica nutans Epilobium ciliatum Conyza canadensis Senecio sylvaticus Carduus crispus Dactylis glomerata Chamaenerion angustifolium Galeopsis tetrahit Lactuca serriola Fallopia dumetorum Galium aparine Calamagrostis arundinacea Carex acutiformis Convallaria majalis Lysimachia vulgaris Carex riparia Phragmites australis Paris quadrifolia Urtica dioica Vincetoxicum hirundinaria Pteridium aquilinum Poa angustifolia Moehringia trinervia Mycelis muralis Hieracium lachenalii Luzula pilosa Festuca ovina Carex digitata Hieracium sabaudum Geranium robertianum Alliaria petiolata Coronilla varia Astragalus glycyphyllos Festuca rubra Euphorbia cyparissias Galium album Lathyrus montanus Silene nutans Linaria vulgaris Deschampsia flexuosa Vaccinium myrtillus Ajuga reptans Scrophularia nodosa Rubus caesius Campanula rotundifolia Rubus saxatilis Veronica chamaedrys

Control B

C

Top

Slope

+° +°

+ 2.1 r 1.1 3.1 +

+ 3.4 + 3.1 . 1.1 /+

+ 4.4 + 3.1 + + +/ 1.1 2.2 1.1 1.1

+ + +

4.4 2.2 +

2.2 + 1.2 + 1.2 + 2.2 + +

1.2 1.1

1.2 2.2

1.2 + + 1.2 + 1.2

2.2 3.4

r

+ + + +

1.2 3.4

1.2 1.2 +

+

1.2 + + + + + +

+ + + + 2.3 1.2 + + + + 2.2

1.1

+

1.2

4.4

+ 2.1 2.1 1.2 1.2 + + + + 1.2 1.2 1.1 + + + + + + + + r

+ + 1.2 + 1.1 2.2 + +

1.2 1.2 + + + + + +

P. Klimaszyk et al. / Science of the Total Environment 517 (2015) 222–231

227

Table 2 (continued) Colony A

Control B

C

Top

Slope

Veronica officinalis Hieracium murorum Polypodium vulgare Cirsium vulgare Mosses Brachythecium rutabulum Pohlia nutans Mnium hornum Polytrichastrum formosum Hypnum cupressiforme Pleurozium schreberi Number of taxa

+ + + r

+

1.2 + +

+ + 2.2 + + 41

+ + 12

12

and exceeded 1500 mg kg− 1 (peripheral colony) or 3000 mg kg− 1 (central and former colony). Deeper-lying soil layers were found to be poorer in nutrients. Nevertheless, their content was always significantly higher than that found at the control site (Table 1). Moreover, soils at the former colony were also rich in nutrients and, particularly in deeper layers, comparable to soils found in the centre of the colony (Table 1). 3.3. Impact on terrestrial vegetation The areas inhabited by cormorants were characterized by different patterns of terrestrial vegetation to these found at the control site (Table 2). No living trees were found at the former colony, instead the forest floor was covered with decomposing Q. petraea and P. sylvestris tree trunks. Nearly 70% of this area was covered with dense standings of Sambucus nigra with the gaps overgrown by tall-herbs such as: Senecio sylvaticus, Poa nemoralis and Epilobium ciliatum. Overall, only 12 plant species were found at the former colony including 3 nitrophilous species: Rubus idaeus, Carduus crispus, S. sylvaticus (Table 2). At the central colony, P. sylvestris and most of the deciduous trees were completely withered. Only a few oaks still possessed leafed branches. The shrub communities were very scattered and limited to a few clusters of S. nigra. More than 70% of this area lacked the herbal layer, the remaining being overgrown by such species as Calamagrostis epigejos, P. nemoralis, S. sylvaticus and nitrophilous Chamaenerion angustifolium. Only 12 plant species were found in this part of the colony (Table 2). The majority of these were profusely covered with cormorant faeces. The peripheral colony was still forested with 6 tree species among which Alnus glutinosa, P. sylvestris and Q. petraea were the most abundant. The herb layer was characterized by grasses and sedges. Convallaria majalis and Urtica dioica were relatively numerous. The moss layer covered nearly 5% of this colony area. Overall, 24 plant species were documented at this site (Table 2). Entirely different and significantly richer vegetation was found at the control site. The highest, flat part was inhabited by 35 plant species while the control island slopes were overgrown by a total of 41 plant species (Table 2) 3.4. Impact on surface runoff Steep inclination of slopes (over 45°) and sparse vegetation contribute to a significant share of the surface runoff in the water balance of the colony area. Surface runoff seems to be the main vector through which the transfer of chemical elements from the colony area to the lake occurs. It was found that surface runoff outflowing from the colony area was characterized by very high nutrient concentrations (Table 3) with mean

24

35

TP content exceeding 17 mg L− 1 and TN over 300 mg L−1 (with a prevalence of organic form). Compared to the control, all chemical parameters were greatly increased: NH4 — 50-fold, NO3 — 30-fold, Norg. over 60-fold, TP — 45-fold. A relatively high DOC content and electrical conductivity, as well as low pH (always below 6.0) were also found. The highest values of the analysed parameters were observed during the breeding season. However, even in the periods when the birds did not occupy the colony area, the concentration of nutrients noted in surface runoff was significantly higher than at the control (Fig. 3). The level of nutrients in runoff largely depended on precipitation and runoff intensity (Fig. 4). The highest content of P and N was found in July 2011 when heavy rainfall occurred after three weeks of dry period — the TP concentration amounted to nearly 40 mg L−1 whereas TN content exceeded 2 g L−1.

3.5. Impact on groundwater The cormorant colony had less effect on groundwater chemistry than it had on surface runoff. Nevertheless, the groundwater at the colony contained significantly increased concentrations of nutrients compared to the groundwater at the control, with TN and TP being Table 3 Physical and chemical properties of surface runoff water under cormorant colony and at control site (n = 21). Mean Colour mgPt L−1 NH4 mgN L−1 NO2 mgN L−1 NO3 mgN L−1 Norg mgN L−1 TN mgN L−1 TP mgP L−1 TRP mgP L−1 DOC mgC L−1 pH el. cond. μSm cm−1

Colony Control Colony Control Colony Control Colony Control Colony Control Colony Control Colony Control Colony Control Colony Control Colony Control Colony Control

312.5 239.5 149.5 2.49 0.07 0.03 27.06 0.9 180.02 2.70 384.7 6.6 17.58 0.4 13.59 0.2 253 63.4

5700.6 132.2

Min

Max

SD

Mann Whitney U test

151.6 162.2 8,7 0.6 0.002 0.001 4.9 0.23 11 2.21 28.9 3.8 8.7 0.07 6.9 0.02 102 26.2 4.18 3.9 894 75

326.2 278.1 1123 4.9 0.4 0.1 60 2.4 1225 2.9 2380.2 9.8 36.2 0.8 30.2 0.41 512 99 5.6 5.9 13,056 300

74.8 41.2 194.2 0.94 0.02 0.01 23.8 0.55 211.4 0.46 510.4 1.19 1.49 0.15 1.32 0.1 26.3 11.4 0.11 0.36 952.6 56.37

Z = 3.1 p b 0.05 Z = 3,7 p b 0.001 Z = 1,7 p N 0.05 Z = 3,73 p b 0.001 Z = 3.7 p b 0.001 Z = 3.5 p b 0.001 Z = 3.8 p b 0.001 Z = 3.77 p b 0.001 Z = 3.22 p b 0.001 Z = −2.2 p b 0.05 Z = 4.2 p b 0.001

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Fig. 3. Mean (±SD) values of DOC (A), electrical conductivity (B), total nitrogen (C) and total phosphorus (D) in surface runoff under the cormorant colony during breeding season and rest of the year.

2-fold and over 4-fold higher, respectively. Moreover, the electrical conductivity of colony groundwater was also increased while the pH was lower (Table 4).

was increased 4-fold (1260 vs 300 μS cm−1). Increased values of the studied parameters in littoral water near the colony were also observed when the birds did not occupy the colony. These amounted to nearly 50% higher TN and over 30% higher TP and TRP concentrations.

3.6. Impact on lake chemistry 3.7. Impact on lake microbiology The colony had a distinct impact on the chemistry of the littoral zone near the island (Table 5). Compared to sites located 50 and 100 m from the colony, and at the centre of the lake, increased values of nearly all parameters were recorded. It is worth noting that the chemistry 50 and 100 m from the colony as well as at the central part of the lake was comparable. The highest concentrations of N and P in the littoral zone were noted during the breeding season, particularly in July 2011, when heavy rainfall occurred after three weeks of dry period. At that time the mean TP concentration was over 30-fold higher than that found at the central part of the lake (3.1 vs 0.1 mg L−1) while TRP was increased over 100-fold (2.1 vs 0.02 mg L−1). Greatly increased values of N forms were also noted at that time: NH4 (2.7 vs 0.3 mg L−1), NO3 (7 vs 0.9 mg L−1) and Norg (21 vs 1.6 mg L−1). Electrical conductivity

As noted, the cormorant colony had an effect on the microbial pollution of lake water. The highest MPN of coliform bacteria and E. coli were observed in the littoral area at the colony and exceeded 950 and 7900 MPN per 100 mL, respectively (Table 5). 4. Discussion The present study clearly demonstrated that cormorants can induce significant chemical and biological transformations of inhabited areas and surface waters adjacent to their colonies by a turnover of matter and energy within and between the ecosystems. As found, the colony exhibited its effects on soil chemistry, overgrowing vegetation, chemical

Fig. 4. The relation between precipitation and total nitrogen (A) and total phosphorus (B) in surface runoff under the cormorant colony. Triangles represent breeding season, circles represent the rest of the year.

P. Klimaszyk et al. / Science of the Total Environment 517 (2015) 222–231 Table 4 Physical and chemical properties of groundwater under cormorant colony and at control site (n = 16). Mean Colour mgPt L−1 NH4 mgN L−1 NO2 mgN L−1 NO3 mgN L−1 Norg mgN L−1 TN mgN L−1 TP mgP L−1 TRP mgP L−1 DOC mgC L−1 pH el. cond. μSm cm−1

colony Control Colony Control Colony Control Colony Control Colony Control Colony Control Colony Control Colony Control Colony Control Colony Control Colony Control

69.32 68.1 3.8 1.97 0.005 0.003 3.46 1.23 5.65 2.87 12.9 6.01 1.02 0.23 0.77 0.12 62.3 69.8

328 281

Min

Max

SD

T test

33.6 29.2 1.8 0.93 0 0 0.98 0.14 2.58 0.98 6.1 3.9 0.26 0.06 0.12 0.02 23 28.2 6.12 5.1 212 201

78.9 77.2 8.9 3.6 0.01 0.002 6.14 2.2 9.11 5.12 19.4 7.8 3.15 0.52 2.65 0.28 112.5 124 7.2 6.59 482.2 368

18.3 22.1 1.74 0.78 0.003 0.004 1.66 0.56 2.25 1.38 1.92 0.76 0.59 0.12 0.59 0.07 26.06 24.23 0.37 0.38 68.72 47.08

t = 1.2 p N 0.05 t = 44 p b 0.001 t = 1.9 p N 0.05 t=6 p b 0.001 t = 5.5 p b 0.001 t = 5.1 p b 0.001 t = 4.9 p b 0.001 t = 4.7 p b 0.001 t = −0.6 p N 0.05 t = 5.8 p b 0.001 t = 2.5 p N 0.001

properties of surface runoff, groundwater and lake littoral. Additionally, the presence of the birds was associated with a significantly increased number of coliform bacteria in the littoral area. Extreme chemical loads deposited by cormorants result from the rapid metabolism of these birds. It has been calculated that each bird can consume 350 g of fish per day (Carss, 1997) and defecate significant amounts of faeces (Kameda et al., 2000; Gwiazda et al., 2010). The mean daily input of droppings can amount to over 30 g dry weight per bird of which more than 80% is deposited directly within the area beneath the colony (Marion et al., 1994). In the present study, the annual nutrient flux with cormorant faeces amounted to 14 g m−2 of N and nearly 8.5 g m−2 of P but was even higher at the central area of the colony. Increased nutrient deposition was also observed within the peripheral colony zone and at the formerly inhabited area. It should be highlighted that the deposition of nutrients with cormorant faeces constitutes only one way through which the birds can fertilize the soil. In addition to excreta, the inhabited areas are characterized by a significantly increased litter fall due to the birds' activities. According to Osono et al. (2006) and Hobara et al. (2001), the cormorants can deposit over 2000 kg ha−1 of forest litter per month. However the present study did not estimate the amount of litter within the colony area, a significant number of dead trees and broken branches were observed at the site of the former colony. Soils within the colony area were found to contain extreme concentrations of N and P, particularly in the surface layer. As demonstrated previously, the nutrient content is usually correlated with the number of birds at the colony (Ligęza and Smal, 2003; Hobara et al., 2005; Rush et al., 2013; Klimaszyk et al., 2015), this pattern was also observed in the present study. The increased chemical content found at the former colony (also within deeper soil layers) highlights that the effect of cormorants on soil transformation (and consequently, biological changes) can be

229

long-lasting. Nevertheless, the content of N at the former colony was lower than in other studied areas — most likely due to the loss of this element through volatilization and elution (Mulder and Keall, 2001; Ligęza and Smal, 2003; Hobara et al., 2005). Moreover, uric acid, a major component of cormorant faeces, can undergo numerous transformations including microbial degradation to ammonia (Ligęza et al., 2001). The chemical transformation of soils at the colony was reflected in changes of terrestrial vegetation. The effect of these birds on plant communities is increasingly being investigated (Hebert et al., 2005; Ellis et al., 2006; Breuning-Madsen et al., 2008; Żółkoś and Meissner, 2008; Boutin et al., 2011). During the early phases of colonization, the constant increase in nutrient content can temporarily promote biomass production and number of plant species due to the higher bioavailability of N and P (Żółkoś and Meissner, 2008). However, at some point, the amount of nutrients exceeds the tolerable level for most species and biodiversity can significantly decrease (Boutin et al., 2011). This is mostly due to altered root absorption capacities in a highly fertile habitat that leads to reduced growth. Seed germination can also be largely affected under such conditions (Ellis et al., 2006; Żółkoś and Meissner, 2008). Increased NH4 concentration can lead to soil acidification (Pearson and Steward, 1993), the conditions under which the uptake of cations is largely altered (VanDijk et al., 1989). Moreover, deposition of faeces directly onto leaves can effectively decrease photosynthetic activity and also lead to retarded growth. Finally, the birds damage tree species mechanically by using their branches and leaves to build nests (Goc et al., 2005). The present study clearly shows that the studied colony limited and modified the terrestrial vegetation. The total number of plant species found at the peripheral, central and former colony was significantly lower than that at the control site. It is worth noting that within the area of the former colony, a spontaneous regeneration of vegetation, represented by a limited number of species, including nitrophilous plants, was observed. An abundant occurrence of S. nigra shrubs decreases the light availability in the floor zone and thereby limits the growth of herbaceous species (Hofmeister et al., 2009). Apart from nitrophilous plants, the former colony was also characterized by three alien species for this geographical zone: E. ciliatum, Conyza canadensis and Lactuca serriola (DAISIE, 2009). It can therefore, be suggested that cormorants can trigger the promotion of species disastrous for European biodiversity. The effect of cormorants is not only limited to terrestrial environments but can be also observed in nearby aquatic ecosystems. The chemical loads deposited by these birds, mainly with faeces, can be at least partially transferred to surface waters through groundwater or surface runoff. Steeply inclined slopes and cormorant-induced deforestation can lead to increased wash-out and transport of N and P, particularly with runoff (Drinan et al., 2013). In the present study, the concentrations of N and P were significantly higher than those found at the control site or within the forested catchment areas not inhabited by cormorants (Klimaszyk and Rzymski, 2011, 2013a; Klimaszyk et al., 2014). Despite the short-term and episodic character of surface runoff, it can constitute a significant share in the water balance and consequently play a key role in external nutrient loading (McDowell et al., 2004; Klimaszyk and Rzymski, 2013a). It has been shown that the highest loads of chemicals are transported during heavy rainfall and snowpack melting (Klimaszyk and Rzymski, 2013a; Klimaszyk and Rzymski, 2014). If the precipitation is preceded by a relatively long

Table 5 Selected physical, chemical (n = 6) and microbial (n = 4) parameters (mean ± SE) of lake water.

Lake near the colony Lake 50 m from the colony Lake 100 m from the colony Central part of the lake a

Data from 2012.

NO3 mgN L−1

Norg mgN L−1

TRP mgP L−1

TP mgP L−1

E. coli a (MPN/100 ml) Coliform a (MPN/100 ml)

pH

el. cond. μSm cm−1

NH4 mgN L−1

6.5–8.2 7.3–8.4 7.1–8.4 7.1–7.9

610 ± 544 312 ± 33 302 ± 21 306 ± 11

0.89 ± 1.2 0.7 ± 3.16 1.7 ± 0.4 0.6 ± 1.3 0.16 ± 0.32 953 ± 303 0.15 ± 0.14 0.52 ± 0.1 0.7 ± 0.1 0.015 ± 0.001 0.033 ± 0.02 12 ± 4 0.12 ± 0.03 0.5 ± 0.1 0.7 ± 0.1 0.015 ± 0.001 0.031 ± 0.01 8 ± 2.2 0.14 ± 0.03 0.53 ± 0.15 0.72 ± 0.11 0.015 ± 0.001 0.032 ± 0.01 8 ± 0.9

7923 ± 2560 451 ± 295 134 ± 32.1 90 ± 17

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dry period, the washing out of chemicals from soil can be magnified (Gupta and Saul, 1996). Such an effect was observed in our study, when in July 2011, heavy rainfall mobilized the nutrients accumulated with cormorant faeces within the colony area. This resulted in a nearly 50-fold increase in runoff concentrations of nutrients. Groundwater was found to play a less significant role in transport of chemicals from the colony to the lake. As previously demonstrated the transfer of N and P from cormorant-affected soils with groundwater is low due to volatilization of the former and low mobility of the latter (Hobara et al., 2005; Osono et al., 2006). On the other hand, if the elevation of ground above lake level is slight, the infiltration of nutrients from the surface soil layers can increase (Klimaszyk, 2012; Klimaszyk et al., 2014). Therefore, at differently situated colonies, the importance of groundwater in nutrient cycling can be higher. As demonstrated, surface runoff can deliver significant loads of nutrients to the lake within a very short period of time, mainly during the vegetative season. Such a phenomenon can lead to fertilization of littoral areas, promote phytoplankton growth and consequently induce eutrophication processes. It was previously found that surface runoff is a very important element of chemical balance for the studied Lake Ostrowiec (Klimaszyk et al., 2014). As estimated, the colony delivers nearly 20% of the total load of N and P to this water body. Despite this, changes in lake chemistry were only found for the zone directly adjacent to the cormorant colony. This is most likely due to the location of the colonized island in the middle of the basin and therefore, strong waving caused by wind leading to rapid dilution of delivered concentrations. If the birds continue to colonize the studied area the effects on the trophic state of the lake can, however, be more explicit. Apart from the chemical changes, the colony can also be responsible for microbial pollution. As shown, many birds can serve as vectors for various bacteria to the aquatic environment, including those that are potentially pathogenic to human and aquatic organisms. The increased numbers of faecal bacteria in waters situated in the vicinity of cormorant colonies can result from the direct deposition of faeces to the lake or the transfer of microorganisms with surface runoff (Klimaszyk, 2012; Klimaszyk and Rzymski, 2013b; Smolders et al., 2014; Gogu-Bogdan et al., 2014). 5. Conclusions The present study demonstrated the complexity through which the effect of cormorant colonies can be manifested. The birds are responsible for the limited growth of terrestrial vegetation through mechanical damage and simultaneous deposition of extreme nutrient loads from their faeces, thereby triggering chemical transformation of soil. Terrestrial fertilization can lead to further chemical transfer to nearby surface waters and the promotion of eutrophication processes. Considering that cormorants can build larger colonies than the one selected for the present study, counting several hundred or thousand breeding pairs, the effects on terrestrial and aquatic environments can in other cases be even more explicit. Nevertheless, even smaller perennial cormorant colonies can induce long-lasting ecosystem modifications. Acknowledgments The research was supported by a grant from the Polish Ministry of Science, No. NN305100435. The authors would like to thank PhD Tomasz Joniak, MSc Piotr Jamrog, and MSc Jarosław Gancarczyk (Drawa National Park) for their help with laboratory and field research and Rob Kippen for proofreading. References APHA, 2005. Standard Methods for the Examination of Waters and Wastewaters, 2005. 21st edition. American Public Health Association, New York. Boutin, C., Dobbie, T., Carpenter, D., Hebert, C.E., 2011. Effect of double crested cormorant on island vegetation, seedbank and soil chemistry: evaluating island restoration potential. Restor. Ecol. 19 (6), 720–727.

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