IRENA TOMÁNKOVÁ1, CHRIS HARROD2,3*, ANTHONY D. FOX4 and NEIL REID1

Reduced primary productivity, macroinvertebrate declines and collapse of overwintering diving duck populations in a large eutrophic lake

IRENA TOMÁNKOVÁ1, CHRIS HARROD2,3*, ANTHONY D. FOX4 and NEIL REID1

1 Quercus, School of Biological Sciences, Queen’s University Belfast, MBC, 97 Lisburn Road, Belfast, BT9 7BL, Northern Ireland, UK

2 School of Biological Sciences, Queen’s University Belfast, MBC, 97 Lisburn Road, Belfast, BT9 7BL, Northern Ireland, UK

3 Instituto de Investigaciones Oceanológicas, Universidad de Antofagasta,Avenida Angamos 601, Antofagasta, Chile

*Correspondence author. E-mail address:

4 Department of Bioscience, Aarhus University, Kalø, Grenåvej 14, DK-8410 Rønde, Denmark

16

Summary

1.  Lough Neagh is one of the most important non-estuarine sites in British Isles for overwintering wildfowl. A state-shift in the waterbird community following the winter of 2000/01 was mostly driven by rapid declines in overwintering diving duck populations. The sudden and discrete changes in the waterbird community on Lough Neagh suggest that they might have been the result of an intrinsic cause.

2.  We investigated changes in density and biomass of benthic macroinvertebrates, the food source for wintering diving ducks and fishes, during 1997/98 (prior to the diving duck population decline) and 2010 (post decline).

3.  The mean total density of macroinvertebrates declined significantly from 15 300 ± 9 487 S.D. individuals m-2 during 1997/98 to 5 136 ± 4 038 individuals m-2 during 2010. Mean total macroinvertebrate biomass declined from 15 667 ± 8 799 S.D. mg m -2 to 5 112 ± 3 759 mg m -2. In terms of taxa composition, the relative contribution of Tanypodinae, Glyptotendipes spp. and Tanytarsini declined while the relative contribution of Chironomus spp. increased.

4.  Primary productivity, as measured by chlorophyll a concentration, was positively correlated with the index for diving duck abundance as well as the total catch of European eels Anquilla anquilla within the system with a lag of one year (Nt-1). Diving duck abundance and the total catch of eels were positively correlated within the same year (Nt). Chlorophyll a concentrations were high during the 1990s but declined throughout the 2000s.

5.  We describe a shift in productivity of the largest freshwater lake in the British Isles which resulted in reduced macroinvertebrate density and biomass with potential implications for ecosystem function and ecologically and economically important consumer populations (diving ducks and fish).

Introduction

Benthic macroinvertebrates are key components of any aquatic ecosystem, providing nutrients and energy to a range of predators, including other invertebrates, fish and birds. Many waterbird species act as predators in freshwater ecosystems, for example, diving ducks feed on benthic macroinvertebrates (Snow & Perrins, 1998). Chironomidae larvae are an important constituent of the diet of lacustrine diving ducks (e.g. Bengtson, 1971; Nilsson, 1972; Winfield & Winfield, 1994b).

As well as their key role in ecosystem function by providing energy and nutrients for consumers, many benthic macroinvertebrate taxa are useful sentinels of environmental change, reflecting their sensitivity to changes in physiochemical conditions or system productivity (Krieger & Ross, 1993; Schloesser, Reynoldson & Manny, 1995; Carter, Nalepa & Rediske, 2006). As indicators of water quality in lake systems, any change in macroinvertebrate abundance or community structure may have profound consequences for the entire ecosystem, including fishes and waterbirds. Thus, since 2000, the Water Framework Directive (Directive 2000/60/EC) has enforced compliance from European Union member states to introduce monitoring and surveillance of inland and coastal water quality including the implementation of measures to maintain ‘favourable conservation status’ at designated sites. Moreover, the EC Birds Directive (2009/147/EC) provides a framework for the conservation and management of wild birds in Europe and confers protection on some waterbirds populations. To fulfil this objective, Member States invariably have site-based waterbird monitoring programmes in place (e.g. Calbrade et al., 2010) to generate population trends in waterbird species.

Lough Neagh (383 km2) is the largest freshwater lake in the British Isles in terms of surface area (Carter, 1993a). It is a Ramsar wetland of international importance, a Special Protection Area (SPA) and an Area of Special Scientific Interest (ASSI). Historically, eutrophication has been a major concern at Lough Neagh (Foy, Lennox & Gibson, 2003), most recently reflecting agricultural run-off (Bunting et al., 2007). Following a large bloom of the blue-green algae Anabaena flosaquae in 1967, human use of the lough was affected by disruption to water treatment plants, fishing industry and recreational use (Wood & Gibson, 1973). Subsequently, Lough Neagh has received considerable scientific attention (e.g. Wood & Smith, 1993) and has been subject to long-term regular water quality monitoring and monthly counts of waterbirds during the winter as part of the national Wetland Bird Survey (WeBS). However, other components of the ecosystem have been less well studied, and there has been no regular monitoring of the benthic macroinvertebrate community beyond the littoral zone, apart from one major survey conducted in 1997/98 (Bigsby, 2000).

Chironomidae larvae are a major component of the lough’s benthic fauna (Carter 1978) and show seasonal variation, with Carter (1976) reporting larval densities of 4 000 individuals m-2 in autumn and 2 000 individuals m-2 in spring. Winfield (1991) gave slightly higher figures, with an average Chironomidae larvae density of 6 250 individuals m-2 in the autumn and 3 275 individuals m-2 in the spring. In 2005, zebra mussels were recorded in Lough Neagh for the first time (McLean et al., 2010); a species that has significantly impacted ecosystem function in lakes throughout Europe and North America (Ward & Ricciardi, 2007). Their impact on Lough Neagh ecosystem has not yet been established as zebra mussel numbers are still low and the species presence localised (McLean et al. 2010).

Previous studies have highlighted the potential for trophic competition between diving ducks, particularly tufted duck, and fish, especially the invasive roach (Rutilus rutilus) for common benthic macroinvertebrate prey (Winfield, Winfield & Tobin, 1992; Winfield & Winfield, 1994). Bigsby (2000) showed some degree of trophic overlap between diving ducks and various fish species but was unable to find any evidence that benthic macroinvertebrate biomass was limiting in terms of availability for predator populations.

Any changes in the macroinvertebrate community due to changes in water quality are likely to have an impact on consumers from higher trophic levels throughout the system, most notably waterbirds and fish. Birds often represent useful indicators of ecosystem change because of statutory monitoring driven by their legislative protection. Indeed, long-term monitoring of waterbirds at Lough Neagh has shown a marked decline in wintering diving ducks, particularly pochard (Aythya ferina), tufted duck (Aythya fuligula) and goldeneye (Bucephala clangula), since the winter of 2000/01 (Tománková et al., 2013). Between the winters of 2000/01 and 2008/09, the overall population of diving ducks on Lough Neagh declined by 63% (Tománková et al., 2013). Different explanations for the causes of these declines have been suggested, including site related factors (Maclean, Burton & Austin, 2006) and migratory short-stopping (Allen & Mellon, 2006; Lehikoinen et al., 2013). Recent research suggests that local factors are likely to be at least partially responsible (Tománková et al., 2013).

Here, we focus on changes in the availability and type of benthic prey available to diving ducks before and after their decline, while simultaneously assessing system productivity through an analysis of chlorophyll a concentrations and eel catches. Specifically, we aimed to: i) describe the contemporary macroinvertebrate community in Lough Neagh in terms of composition and abundance in order to assess food resource availability for top consumers, including diving ducks and fishes, and ii) to assess temporal changes in the composition and abundance of benthic macroinvertebrate community between the winters of 1997/98 (Bigsby, 2000) and 2010 (this study).

Methods

Study site

Despite its large surface area, Lough Neagh (54˚35'N, 6˚25'W) is relatively shallow, with a mean depth of 9 m; as a consequence it usually remains well-mixed and the water column is typically well oxygenated (Carter, 1993a). Lough Neagh drains a large part of the north of the island of Ireland, with six inflowing rivers and a single outflow river that drains into the Atlantic Ocean. The catchment is primarily agricultural, dominated by dairy and beef farming (Carter, 1993b).

Macroinvertebrate surveys

In the absence of routine macroinvertebrate surveys, we compared densities and biomass with the last most detailed study of the lough made prior to the decline in diving duck populations (Bigsby, 2000). This involved core sampling macroinvertebrate communities inhabiting soft sediments in 6 bays (Washing Bay, Kinnego Bay, Bartin’s Bay, Lennymore Bay, Antrim Bay and Ballyronan Bay) at depths ranging from 3 to 12m (Fig. 1) during October and January. These months were selected to represent the period reflecting the use of the lough by the overwintering diving ducks. The previous survey covered the winter of 1997/98, while the current study was conducted in January and October 2010. Repeated samples (n = 5) of sediment were taken at each depth with a Kajak corer (21.23cm2) attached to either a rope or a hand pole. This method was unlikely to effectively sample more mobile macroinvertebrates, such as Gammarus spp., Asellus aquaticus and Mysis spp. due to their rapid escape behaviours and therefore their numbers are likely to have been underestimated. However, since the main purpose was the comparison of the macroinvertebrate fauna of Lough Neagh between two time periods, this issue was deemed not relevant. Samples were washed through a 250 µm sieve to remove sediment. Macroinvertebrates were then picked out, counted and identified. In most cases, Chironomidae larvae head capsules were mounted with either Euparal or Hydromatrix solutions (Brooks, Langdon & Heiri, 2007) to allow identification (Wiederholm 1983; Brooks et al., 2007). Not all macroinvertebrates were identified to species; instead, operational taxonomic units were used. This was particularly the case for Chironomidae larvae which were generally identified to genus level, and Trichoptera larvae which were identified to family level. Although relatively abundant, oligochaeta were excluded from the survey following Bigsby (2000). Rare taxa were grouped in the category “other”.

All macroinvertebrates were measured to allow biomass to be estimated. Total length ± 0.001 mm was typically recorded but occasionally, head capsule dimensions were taken for Chironomidae larvae, if only part of the body was found in the sample. Mass-length regressions were then used to convert body dimensions into biomass. The regressions for Chironomidae larvae, Asellus aquaticus, Gammarus spp. and leeches were taken from Bigsby (2000), while regressions for all other macroinvertebrate taxa were obtained from Benke et al. (1999). Mysis were weighed due to the low number of individuals sampled. Both macroinvertebrate counts and dry mass were converted into estimates of density (individuals m-2) and biomass (mg m-2).

Data from the 1997/98 survey (Bigsby 2000) were extracted from graphs using Plot Digitizer (version 2.5.1) software, as the original raw data could not be retrieved in any other form. These values were then converted to density (individuals m-2) and biomass as dry mass (mg m-2) to permit comparison.

Productivity and eel data

Levels of chlorophyll a (µg L-1) at Lough Neagh were measured from 1995 to 2011. Ten metre composite water samples were collected fortnightly using a flexible tube from a central location in Lough Neagh (54o37’N, 6o24’W) and averaged for each year. Chlorophyll a was measured after extraction into hot (55°C) methanol (Talling, 1969).

The total annual catch of eels (both resident yellow and migratory silver phases) were obtained for the period 1995 to 2011 based on census techniques described by Rosell, Evans & Allen (2005). Both productivity and fish data were obtained from the Agri-Food and Biosciences Institute (AFBI), Northern Ireland.

Statistical analysis

Variation in total macroinvertebrate abundance and dry mass was examined using Generalized Linear Mixed Models (GLMMs), using a negative binomial distribution with a log link function to account for the large variance of data relative to the mean. Transect ID was fitted as a random factor to account for multiple observations at each sampling site. Survey period, Depth and Season were fitted as fixed factors. Statistics were conducted using SPSS v20 and graphs plotted using Sigmaplot v10.

In order to characterise how the overall macroinvertebrate community changed between the two survey periods, we undertook a parallel multivariate analysis. Here, the total abundance of each macroinvertebrate taxon was summed for each survey, segregating data by depth (3, 6, 9, and 12 m) and survey transect (Antrim, Ballyronan, Bartin's, Kinnego, Lennymore and Washing Bays). Abundances were square-root transformed and standardised before a Bray-Curtis dissimilarity matrix was constructed using PRIMER 6.1.13 and PERMANOVA 1.0.3 (Anderson, Gorley & Clarke, 2008). Spatial (Transect, Depth) and temporal (Season, Survey period) influences on the relative abundance of macroinvertebrate taxa were examined using a four-way permutational (n permutations = 9 999) multiple analysis of variance (PERMANOVA). Transect ID was fitted as a random factor and Depth, Survey and Season were fitted as fixed factors. Following the PERMANOVA analysis, we examined those taxa driving the key differences in survey periods using the SIMPER in PRIMER.

Variation in community structure associated with survey period and sample depth was graphically visualised using a Principal Coordinates Analysis (PCO); an unconstrained ordination method also known as metric multi-dimensional scaling (Anderson & Willis, 2003; Anderson et al., 2008). We included vectors based on multiple correlation (correlation coefficients >0.4) to highlight those taxa driving the distribution of data along the first two PCO axes, whilst accounting for variation in the other taxa.

Concentrations of chlorophyll a were tested before and after the known change point in the temporal trend for diving duck abundance (Tománková et al., 2013) using a t-test (i.e. pre- and post-2001).

Relationships between mean chlorophyll a, the total annual catch of eels and the diving duck index were examined using cross-correlations (Pearson’s r) at various temporal lags.

Results

Total macroinvertebrate density decreased by two thirds between 1997/98 and 2010 (Table 1 and Fig. 2a-d), with an estimated mean ± SD density of 15 300 ± 9 487 individuals m-2 during 1997/98, compared to 5 115 ± 3 944 individuals m-2 during 2010. Total macroinvertebrate dry mass also decreased by an order of magnitude between the survey periods (Table 1 and Fig. 2e-h), from a mean ± SD dry mass of 15 667 ± 8 799 mg m-2 in 1997/98 to 5 275 ± 3 751 mg m-2 in 2010. Both measures of total density and biomass were higher in October than in January (Table 1 and Fig. 2). Total density of macroinvertebrates also varied significantly with depth (Table 1). Zebra mussels were not recorded in the current survey; however, it is likely that the species would be under-sampled on soft sediments.