Biogeography and fish community structure in Irish estuaries

Regional Studies in Marine Science 32 (2019) 100836

Contents lists available at ScienceDirect

Regional Studies in Marine Science journal homepage: www.elsevier.com/locate/rsma

Biogeography and fish community structure in Irish estuaries ∗

Lynda Connor , Diarmuid Ryan, Rory Feeney, William K. Roche, Samuel Shephard, Fiona L. Kelly Inland Fisheries Ireland, 3044 Lake Drive, Citywest Business Campus, Dublin 24, Ireland

article

info

Article history: Received 14 March 2019 Received in revised form 13 September 2019 Accepted 14 September 2019 Available online 19 September 2019 Keywords: Transitional waterbodies Biogeography Irish coast Fish community structure Ecosystem characteristics Environmental variables

a b s t r a c t Estuaries represent important transitional waters where marine and freshwater ecosystems meet and mix. Estuaries are dynamic systems due to their tidal nature and their ecology is expected to shift with climate change and the arrival of new species. Spatially extensive descriptive studies that provide temporal baselines for species distribution and abundance, and associated environmental variables deliver a comprehensive reference point against which to monitor change. To provide this biogeographic context for Ireland, which is surrounded by temperate Atlantic waters, the biogeography and fish community structure of Irish estuaries was examined using a large dataset comprised of 208,313 individual fish, 80 different species sampled from 37 estuaries from 2008–2017. Species richness was strongly correlated with the area of shallow littoral and subtidal habitats. Estuaries at higher latitudes tended to have lower species richness in shallow littoral areas. Estuary mouth width and proportion of subtidal area were both positively related to species richness in subtidal habitats. The main driver of estuary clustering is the changing proportion of estuarine species versus marine migrants. The results show a dominant group of larger, more open estuaries where marine migrants consistently dominate the fish population. This study confirms the role of marine migrants in contributing to fish community composition in estuaries and highlights the vital nursery function that Irish estuaries perform for estuarine-dependent marine fish species. The associations between fish community structure and broad-scale environmental parameters provide a time stamped baseline for monitoring future climate change impacts on estuarine fish assemblages in Ireland. © 2019 Elsevier B.V. All rights reserved.

1. Introduction Estuaries are partly-enclosed coastal bodies of water receiving one or more rivers or streams and an unhindered connection to coastal waters (NOAA, 2019). These habitats form a transition zone between freshwater river and saline ocean environments, where ecological successions can form along the environmental gradient. Estuaries are subject to both marine influences, such as tides, waves, and the influx of saline water, as well as riverine influences, such as flows of freshwater and sediment. The inflow of both seawater and freshwater provide high levels of nutrients in the water column and sediment, making estuaries fertile and productive natural habitats for the plants and animal species inhabiting them (NOAA, 2017). Estuarine fish communities vary greatly at different spatial and temporal scales due to the highly variable estuarine environment encompassing salinity gradients, shallow depths, muddy grounds, high turbidity, and subtidal and intertidal areas, which provide ∗ Corresponding author. E-mail address: [email protected] (L. Connor). https://doi.org/10.1016/j.rsma.2019.100836 2352-4855/© 2019 Elsevier B.V. All rights reserved.

essential habitats for diverse fish species (Nicolas et al., 2010). Many fish species benefit from the highly productive nature of estuaries for all or part of their life cycle. Fish communities in estuaries are comprised of species resident in the estuary, marine and freshwater species which enter and inhabit estuaries adventitiously either as migrants or as stragglers, freshwater species that inhabit the freshwater tidal reaches, diadromous species that pass through estuaries en route to feeding and breeding grounds elsewhere (Elliott et al., 2007) and species on their migratory route within an estuary or on their journey from freshwater to sea. Some fish migrate through estuaries: anadromous species like Atlantic salmon (Salmo salar) and lamprey (Petromyzontiformes) migrate through estuaries from the sea to reach freshwater spawning grounds, whereas European eel (Anguilla anguilla) are catadromous, migrating down through estuaries as adults to spawn in oceanic waters. The tidal freshwater reaches of estuaries form important staging points for juvenile anadromous and catadromous species, giving them time to form social groups (Henkel, 2015) and to acclimatise to changes in salinity. At times, there may be only a small number of resident fish species present in an estuary, but seasonal migrants and some forage fish

2

L. Connor, D. Ryan, R. Feeney et al. / Regional Studies in Marine Science 32 (2019) 100836

such as herrings (Clupea harengus) and sprats (Sprattus sprattus), occasionally increase species diversity in the lower reaches of the estuary (Kültz, 2015). Besides the species that migrate through estuaries, many others use them as nursery grounds for spawning or as sub-adult feeding grounds (Haedrich, 1987; McHugh, 1967). For species that can tolerate changing conditions, the lower abundances of some marine predators and a rich particulate food supply in estuaries make these systems attractive spawning and nursery grounds for many species that normally live under full salinity conditions (Haedrich, 1987; McHugh, 1967), such as commercial angling species like cod (Gadus morhua) and sole (Solea solea). Herring and plaice (Pleuronectes platessa) are both commercially important species that can spawn in lower estuaries (Jovanovic et al., 2007; McLusky et al., 1990), where salinity conditions are favourable. Species richness in estuaries follows a well-understood pattern along the salinity gradient described by Remane (1934). True estuarine species are those that complete their whole life cycle within the transitional waters (Potter et al., 2013). Transitional waters are defined as ‘bodies of surface water in the vicinity of river mouths which are partially saline in character as a result of their proximity to coastal waters but which are substantially influenced by freshwater flows’ (McLusky and Elliott, 2007). These are typically hardy, stress-tolerant species able to tolerate salinity shifts and high levels of suspended solids (Kültz, 2015). Moving down an estuary, freshwater species become less abundant with increasing salinity and are gradually replaced by marine organisms, with some true estuarine species found at intermediate salinities (Telesh and Khlebovich, 2010). This pattern is reflected by the overall species richness, where the least diverse fauna is found at salinity levels of between 5 and 18 PSU (Sosa-López et al., 2007). Rising sea levels as a result of global climate change are likely to intensify saline intrusions into freshwater ecosystems (Schallenberg et al., 2003), and can be expected to change this salinity-species gradient. It is known that some fish species are well distributed in Irish estuaries, e.g., Sprattus sprattus (sprat), Platichthys flesus (flounder), Pomatoschistus microps (common goby), Salmo trutta (brown trout/sea trout), Anguilla anguilla, Ciliata mustela (five-bearded rockling), Pleuronectes platessa (plaice), Pollachius pollachius (pollack) and Chelon labrosus (thick-lipped grey mullet) (Went, 1978). In a study carried out in Dublin Bay in 2005, the community was found to be largely dominated by the Ammodytes tobianus (lesser sandeel) and common goby (Jovanovic et al., 2007). Although there are studies on estuarine fish communities in other temperate waters (Araújo et al., 1998, 2000; Cabral, 2000; Cabral and Costa, 2001; Claridge and Potter, 1983, 1984, 1985, 1987; Elliott and Taylor, 1989; Greenwood et al., 2002; Harrison and Whitfield, 2006a,b,c; Henderson and Bird, 2010; Jorge et al., 2002; McLusky et al., 1990; Power et al., 2000; Lepage et al., 2016), there is a recognised paucity of more recent literature reviewing the current fish community structure of Irish estuaries (Harrison et al., 2017). Wilson et al. (2016) compared the fish communities of nine Irish estuaries, but this was restricted to the tidal freshwater zone only. Most studies tend to focus on a particular species or estuary, whereas this study is all encompassing — all species countrywide. Estuaries are important transitional waters where marine and inland systems meet and mix. The ecology of estuaries is expected to shift with climate change and the associated arrival of new species. Spatially extensive descriptive studies, like the current study, that provide temporal baselines for species distribution and abundance, and associated environmental variables deliver a comprehensive reference point against which to monitor change (Lepage et al., 2016; Breine et al., 2011). Outlining the associations between community structure and broad-scale environmental

Fig. 1. Location map of estuary systems in this study.

parameters provides a baseline for monitoring future environmental and climate change associated impacts on estuarine fish assemblages in Ireland. The aims of the current study were (1) to provide a baseline description of the fish species currently present in Irish estuaries, and (2) to analyse the relationships between fish species richness and relative abundance of functional groups, and the physical characteristics of estuaries around the island of Ireland. We also highlight a number of the rarer species encountered. 2. Material and methods 2.1. Study area The study area consisted of 37 estuaries (Fig. 1) located around Ireland—an island with a coastline of approximately 7500 km surrounded by temperate Atlantic waters and positioned on the north-western edge of Europe. These were delineated by the Environmental Protection Agency as an outcome of the Article 5 Characterisation report (EPA, 2005, 2006). These systems were defined on the basis of individual transitional waterbodies or the aggregation of contiguous transitional waterbodies in the case of large estuaries that are subdivided into multiple waterbodies, e.g., the Shannon Estuary (Fig. 1) as per the typology systems described within the Water Framework Directive (WFD) and European Union Common Implementation Strategy Guidance (EU CIS Guidance) (EC, 2019). Coastal and transitional lagoons that did not have a direct, permanent connection to the sea or to another transitional waterbody were not included in the analysis, as many of these systems are unlikely to serve as important habitat for estuarine-associated fishes (Bamber, 2010). 2.2. Fish surveys Fish stock surveys were conducted annually around the Irish coast in Autumn (September to November) using standard European methodology (CEN, 2005) on a rolling three year basis as

L. Connor, D. Ryan, R. Feeney et al. / Regional Studies in Marine Science 32 (2019) 100836

3

Fig. 2. Mean species richness in the shallow littoral zone (beach seines) for all years surveyed.

part of the national programme of fish monitoring for the WFD between 2008 and 2017 by Inland Fisheries Ireland (IFI) (Kelly et al., 2009, 2010, 2011, 2012, 2013, 2014, 2015; Ryan et al., 2016, 2017, 2018). Between 2008 and 2017, 19 of the estuaries were surveyed in one year, 12 in two years and 8 on three occasions, giving a total of 67 surveys for analysis. A standard multi-method sampling approach was used to sample fish in Irish transitional waters for national reporting on the Water Framework Directive (WFD) (CEN, 2005; Coates et al., 2007; Harrison and Kelly, 2013); this consisted of seine netting, fyke netting and beam trawling. The two different sampling methods analysed in this study are described below, these methods surveyed the two main habitat types. Seine netting was conducted using a 30 m long × 2 m deep seine net, with a 14 mm mesh body with a 5 m long × 6.5 mm central panel. Fyke netting was conducted using double-ended fyke nets that consisted of two traps measuring 0.5 m high, 2.5 m long with a 10 mm mesh cod end that were joined by a 8 m long × 15 mm mesh leader; these fyke nets were set in groups of three tied end-to-end. Seine netting was conducted in shallow, usually <1.5 m deep, littoral zones, while the fyke nets were set for 24 h in the subtidal benthic zones (to ensure water coverage at all times). Sampling effort is not directly comparable between the two methods due to differing catchability for certain fish species; therefore, methods were analysed separately and the output was described in the context of habitat type, i.e. shallow littoral and subtidal. Sampling effort (number of samples and deployment of the different gear types) was adjusted among estuaries to ensure adequate coverage of each waterbody (Harrison and Kelly, 2013). Representative habitats were qualitatively identified in each system based on factors such as exposure/orientation, shoreline slope and substrate type; these strata were then sampled using both gear types. A handheld GPS unit was used to mark the precise location of each site. Where possible, all fish were identified to species level and counted in the field and returned alive to the water. Length measurements were recorded for each species using a representative

Fig. 3. Relationship between species richness and selected environmental variables in the shallow littoral zone of Irish estuaries. Only statistically significant regressions are presented. Each sample (n = 62) represents species richness calculated from beach seine data, in an estuary in a particular year (2008–2016).

sub-sample, while scales were only collected for certain species, including salmon, sea bass (Dicentrarchus labrax) and sea trout. Fish specimens that were difficult to identify in the field were retained for subsequent identification in the laboratory (Harrison and Kelly, 2013). For the sub sample of fish for which lengths were measured, individual fish were categorised as juvenile or adult on the basis of length-at-maturity values obtained from Heessen et al. (2015), IFCA (2017), Petr (1999), Fish (1989), Monteiroa et al. (2005), Metin et al. (2011) and Froese and Pauly (2018). 2.3. Estuary characteristics/environmental variables GIS software ArcMap 10.3.1 was used to intersect the estuary systems with available geographical and physicochemical data to develop a suite of 37 environmental variables that potentially influence estuarine fish communities (Table 1). Using metrics described by McGarigal et al. (2002) and Meynecke et al. (2008), topographical variables that describe estuary shape, exposure and connectivity to the sea were also calculated to investigate the potential influence of seascape on estuarine fish communities. The estuary areas were delineated based on the WFD waterbody shapefiles available for download from the Environmental Protection Agency Geoportal located at http://gis.epa.ie/GetData/ Download. 2.4. Data analysis 2.4.1. Explanatory variable selection Many of the 37 environmental variables collated are likely to be correlated. Following the protocol described by (Zuur et al., 2010), Spearman correlation analyses (R Core Team, 2017) were

4

L. Connor, D. Ryan, R. Feeney et al. / Regional Studies in Marine Science 32 (2019) 100836

Table 1 Estuarine environmental variables and descriptors that were subjected to initial exploratory analysis. Variable

Units

Description

Latitude Longitude Estuary area Length coast Estuary mouth width Mean distance to sea MouthWidth:Area MouthWidth:Distance To Sea Shape index Sinuosity index Coast:Area ratio Fetch index Offshore wind speed Shelf distance Catchment area Upstream river channel Upstream river flow Inflowing rivers Shreve input Average annual rainfall Mean source elevation Intertidal area Subtidal area Saltmarsh habitat Ecological status Salinity range Annual mean salinity Annual mean BOD Annual mean TON Annual mean NH3 Annual mean PO4 Annual mean chl_a Coastal dredge fishing Median depth Mean tidal range Tidal prism volume Halocline

degrees degrees ha km m m ratio ratio index index ratio index m/s km km2 km m3 /s count total mm m proportion proportion proportion category psu psu mg/l O2 mg/l N mg/l N µg/l P mg/m3 proportion m m km3 binary

Latitude Longitude Area Length of terrestrial coastline along estuary boundary Length of the boundary between estuary system and adjoining WFD coastal waterbody Least cost distance to sea calculated from estuary mouth up through the estuary system Ratio of the estuary mouth width to the estuary area Ratio of estuary mouth width to mean distance to sea Estuary perimeter divided by the square root of estuary area, multiplied by a constant Coastal tortuosity from straightness (=1). Mean coastal segment length divided by chord Ratio of length of terrestrial coastline to estuary area Mean of the products of fetch distance on bearings and the wind energy for each bearing Mean wind speeds at 50 m over estuary waterbody Least distance from estuary centroid to continental shelf at 200-metre depth contour Upstream freshwater catchment area Upstream freshwater channel length 95th percentile flow in cumecs at nearest upstream hydrometric station Number of inflowing rivers and streams inflows River discharge into estuary calculated as total Shreve value for inflowing rivers Annual rainfall in upstream catchment based on Met Éireann 1981–2010 climate average Mean elevation of all 1st order stream sources flowing into estuary Percentage of estuary area that is intertidal based on OSi Discovery series mapping Percentage of estuary area that is subtidal based on OSi Discovery series mapping Percentage of estuary area that is saltmarsh based on NPWS mapping Overall ecological status 2010–2012 as reported by the EPA from high (5) to bad (1) Range of salinity (psu) recorded 2007–2013. EPA data Annual mean salinity (psu) recorded 2007–2013. EPA data Annual mean biochemical oxygen demand (mg/l O2 ) recorded 2007–2013. EPA data Annual mean total oxidised nitrogen (mg/l N) recorded 2007–2013. EPA data Annual mean total ammonia (mg/l N) recorded 2007–2013. EPA data Annual mean molybdate reactive phosphorus (µg/l P) recorded 2007–2013. EPA data Annual mean chlorophyll a (mg/m3 ) recorded 2007–2013. EPA data Percentage area of dredge fishing in estuary and within 10 km seaward buffer. MI data Median depth of estuary area. EPA data Mean tidal range = (mean high spring/high neap) − (mean low spring/low neap). EPA data Volume of water between mean high tide and mean low tide. EPA data Halocline present in the system. EPA data

Table 2 Explanatory environmental variables used in linear mixed models of the fish community in Irish estuaries. Estuary name and sampling year we applied as random effects on the intercept. Variable

Units

Mean (s.d)

Min.

Max.

Latitude Estuary mouth width MouthWidth:Area Fetch index Estuary area Subtidal area Estuary name Sampling year

decimal degrees metres metres:hectares unitless index hectares proportion random effect random effect

53.058 (1.026) 1688 (2057) 2.078 (2.432) 7.658 (17.443) 1693.9 (3810.8) 0.498 (0.259)

51.527 11 0.192 0.216 11.8 0.092

55.041 9841 12.843 111.782 24061.1 1

carried out between variables, and those with a high correlation coefficient (r > 0.7) were removed to limit multicollinearity between variables. All variables describing upstream catchment (Shreve, catchment, river inflows, river length) were highly correlated with estuary area, and were omitted from further analyses (Zuur et al., 2010). Preliminary analysis indicated that chemical variables did not explain much variation in fish community composition and these were also excluded. Salinity sampling techniques were not standardised between estuaries and years; values were largely related to where within the estuary and at what time of the tide sampling was carried out and these data were excluded. A final set of six continuous explanatory variables were retained (Table 2):

Fig. 4. Mean species richness in the subtidal zone (fyke netting) for all years surveyed.

Model

Covariate 1

Covariate 2

Covariate 3

Covariate 4

Covariate 5

Covariate 6

AIC-Sp richness Seine

AIC-Sp richness Fyke

AICmarine migrant seine

AICmarine migrant fyke

AICestuarine species seine

m1(full model) m2 m3 m4 m5 m6 m7 m8 m9 m10 m11 m12 m13 m14 m15 m16 m17 m18 m19 m20 m21

Latitude

Estuary mouth width

MouthWidth:Area

Estuary area

Fetch index

Subtidal area

354.9

332.4

844.8

496.0

848.7

Latitude Estuary mouth width MouthWidth:Area Estuary area Estuary mouth width Estuary area Estuary area Subtidal area Fetch index Subtidal area Fetch index Latitude Subtidal area Subtidal area Subtidal area Estuary area Estuary mouth width MouthWidth:Area Latitude MouthWidth:Area

MouthWidth:Area MouthWidth:Area Estuary mouth width Estuary mouth width Estuary area MouthWidth:Area Estuary mouth width Estuary area Estuary area MouthWidth:Area Estuary area Estuary mouth width MouthWidth:Area Latitude Fetch index Estuary area

MouthWidth:Area Estuary mouth width Estuary mouth width Estuary mouth width MouthWidth:Area Latitude Fetch index Estuary area Subtidal area

378.7 382.3 373.8 369.3 367.9 364.1 371.2 383.3 371.2 370.6 383.5 355.7 372.3 364.0 368.3 354.0 359.9 355.1 368.4 361.9

364.0 356.7 361.2 345.6 345.9 346.6 344.3 355.8 346.7 356.0 358.1 348.6 342.7 334.5 344.0 342.0 349.5 348.0 346.2 330.2

844.7 841.1 846.6 839.9 841.2 841.7 839.5 842.8 841.9 847.8 841.5 841.7 841.3 842.4 841.4 841.0 842.2 843.6 843.6 842.9

496.2 492.9 494.8 497.0 494.0 496.5 494.1 491.6 498.2 492.4 494.9 497.1 492.8 490.9 494.7 496.6 496.3 499.1 499.7 492.9

859.6 856.6 861.9 858.6 856.7 860.6 857.4 849.4 860.0 853.1 853.5 860.1 850.0 846.8 851.0 857.1 854.5 861.8 853.3 848.8

m22

Fetch index

Estuary area

Subtidal area

Latitude

370.3

346.0

843.1

496.5

848.8

m23 m24 m25

Subtidal area Estuary mouth width Latitude

Estuary mouth width Latitude MouthWidth:Area

Latitude MouthWidth:Area Estuary mouth width

Fetch index Estuary area Subtidal area

358.6 355.0 354.3

337.2 343.5 331.5

844.0 842.9 843.0

494.0 498.2 494.7

846.7 856.5 849.5

Latitude Latitude Fetch index Estuary area Subtidal area Estuary mouth width Estuary mouth width MouthWidth:Area Fetch index Estuary area

L. Connor, D. Ryan, R. Feeney et al. / Regional Studies in Marine Science 32 (2019) 100836

Table 3 List of covariate combinations examined within generalised linear mixed effects models used to test which best explained variation in the response variable between estuaries. All AIC values for ∆AIC ≤ 4 highlighted in bold. For covariate and random effect details, refer to Table 1.

5

6

L. Connor, D. Ryan, R. Feeney et al. / Regional Studies in Marine Science 32 (2019) 100836

Table 4 Relative abundance of functional groups across all estuaries and years. Functional group

Method

Relative abundance

Max

Min

Standard deviation

Marine migrants

Fyke Seine

0.77 0.36

1.00 0.98

0.17 0.00

0.19 0.30

Marine stragglers

Fyke Seine

0.07 0.04

0.65 0.92

0.00 0.00

0.13 0.14

Estuarine species

Fyke Seine

0.02 0.48

0.15 0.99

0.00 0.01

0.03 0.30

Diadromous species

Fyke Seine

0.14 0.01

0.64 0.08

0.00 0.00

0.15 0.02

Freshwater migrants

Fyke Seine

0.00 0.09

0.10 0.81

0.00 0.00

0.02 0.20

Freshwater stragglers

Fyke Seine

0.00 0.02

0.02 0.40

0.00 0.00

0.00 0.08

1. Latitude was calculated in decimal degrees for the centroid of each estuary. 2. Estuary area (ha) was calculated from the WFD waterbody shapefiles and summed to give the total area of each estuary system. 3. Estuary mouth width (m) was defined as the length of the boundary between each estuary system and the adjoining coastal waterbody as defined by the EPA. 4. Subtidal area was calculated as the percentage of the estuary area. 5. MouthWidth:Area is the ratio of the estuary mouth width (m) to the estuary area (ha). This variable was calculated as an indicator of how open an estuary is to the sea relative to its connection to adjacent coastal waters. This ratio tends to be lower in larger estuaries with a relatively narrow mouth and higher in smaller estuaries with a relatively wide mouth. 6. Fetch index is a topographical index adapted from the work described by Burrows et al. (2008), Malhotra and Fonseca (2007) to characterise the effects of wave exposure on rocky shore communities. For each estuary system, the fetch distance (m) was calculated over vectors at bearings of 30◦ intervals at 1 km intervals along the coastline to a maximum of 200 km, at which wave conditions can be considered fully developed (Harborne et al., 2006). The fetch index for each estuary is the mean of the products of fetch distance on all bearings and the wind energy for each of these bearings. The wind energy is the product of the proportion of time the wind blew on a given bearing and the square of the average wind speed (knots) on that bearing. The wind data was derived from hourly weather station data downloaded from the Met Éireann website at https://www.met.ie/climate/availabledata/historical-data, and each estuary was matched to the wind data for the closest synoptic weather station within 20 km of the coast. The fetch index was calculated as an indicator of the degree to which each estuary is open to waves or sheltered, taking into account whether the estuary is long and narrow or more open and whether the estuary mouth is wide or narrow and whether it exposes the estuary to prevailing winds. Generalised Linear Mixed Effect Models (GLMM) (Bates et al., 2015) were used to explore important environmental variables driving estuarine fish species richness and relative abundance. Ordination was then applied to explore community patterns among estuary groupings.

Fig. 5. Relationship between species richness and selected environmental variables in the subtidal zone of Irish estuaries. Only statistically significant regressions are presented. Each sample (n = 62) represents species richness calculated from fyke net data, in an estuary in a particular year (2008–2016).

2.4.2. Species richness Generalised Linear Mixed Effect Models (GLMM) with a Poisson distribution (Zuur et al., 2007) were fitted to examine variation in fish species richness associated with variation in geomorphic/physical characteristics among estuaries around Ireland. Fyke nets and seine nets were considered separately, with a duplicate modelling process for each gear type. Twenty-five candidate GLMMs were built using various combinations of the six explanatory variables (Table 3) that were anticipated to be important. Variation between estuaries and sampling year was accounted for by adding random effects, ‘‘estuary name’’ and ‘‘sampling year’’ on the intercept. All explanatory variables were scaled to have zero mean and unit variance prior to analysis so that the magnitudes of model coefficients can be directly compared (Gelman, 2008). The best models were selected according to the Akaike Information Criterion (AIC) (Burnham and Anderson, 2002), whereby, only the models with the lowest AIC values (∆AIC ≤ 4) were subject to further consideration. Within this subset, the model with the least number of uninformative parameters (p ≥ 0.01) was selected as the final model (Arnold, 2010). In order to describe the predictive capacity of each final model, marginal and conditional R2 values were estimated using the MuMIn package (Barton, 2018) in R. This procedure is based on the Nakagawa et al. (2017) paper. Sp_richnessij ∼ Poisson(µij ) Log(µij ) = β1 + β2 X Latitudeij + β3 X Estuary mouth widthij

+ β4 X MouthWidth:Areaij + β5 X Estuary areaij + β6 X Fetch indexij + β7 X Subtidal areaij + αi + εj

L. Connor, D. Ryan, R. Feeney et al. / Regional Studies in Marine Science 32 (2019) 100836

7

Table 5 Fish species encountered with guilds, percent frequency of occurrence (%) and percent of juveniles captured (%) in Irish estuaries (seines and fykes, 2008–2017). The functional guilds are freshwater migrants (FM), marine stragglers (MS), freshwater stragglers (FS), estuarine species (ES), diadromous species (DI) and marine migrants (MM). The feeding guilds are zoobenthivores (ZB), piscivores (PV), zooplanktivores (ZP), detritivores (DV) and omnivores (OV). Species

Common name

ID

Functional guild

Feeding guild

% occurrence

% juveniles

Trachurus trachurus Labrus bergylta Trisopterus luscus Gobius niger Scophthalmus rhombus Scyliorhinus stellaris Pollachius virens Gadus morhua Callionymus lyra Pomatoschistus microps Liparis liparis Solea solea Conger conger Crenilabrus melops Labrus mixtus Limanda limanda Leuciscus leuciscus Syngnathus typhle Anguilla anguilla Dicentrarchus labrax Spinachia spinachia Ciliata mustela Platichthys flesus Sparus aurata Chelon auratus Ctenolabrus rupestris Syngnathus acus Hyperoplus lanceolatus Eutrigla gurnardus Gobio gobio Pholis gunnellus Melanogrammus aeglefinus Clupea harengus Lampetra sp. Ammodytes tobianus Scyliorhinus canicula Echiichthys vipera Hippoglossoides platessoides Taurulus bubalis Cyclopterus lumpus Scomber scombrus Phoxinus phoxinus Syngnathus rostellatus Pungitius pungitius Pomatoschistus pictus Perca fluviatilis Esox lucius Pleuronectes platessa Agonus cataphractus Pollachius pollachius Trisopterus minutus Lampetra fluviatilis Rutilus rutilus Centrolabrus exoletus Gobius paganellus Scardinius erythrophthalmus Salmo salar Pomatoschistus minutus Atherina presbyter Solea lascaris Salmo trutta Lipophrys pholis Myoxocephalus scorpius Osmerus eperlanus Mustelus mustelus Entelurus aequoreus Sprattus sprattus Barbatula barbatula Mullus surmuletus Chelon labrosus Chelon ramada

Atlantic horse mackerel/Scad Ballan wrasse Bib Black goby Brill Bull huss Coalfish (Saithe) Cod Common dragonet Common goby Common seasnail Common sole Conger eel Corkwing wrasse Cuckoo wrasse Dab Dace Deep-snouted pipefish European eel European sea bass Fifteen-spined stickleback Five-bearded rockling Flounder Gilthead bream Golden grey mullet Goldsinny wrasse Greater pipefish Greater sandeel Grey gurnard Gudgeon Gunnel (Butterfish) Haddock Herring Lamprey sp. Lesser sandeel Lesser spotted dogfish Lesser weever Long rough dab Long-spined sea scorpion Lumpsucker Mackerel Minnow Nilsson’s pipefish Nine-spined stickleback Painted goby Perch Pike Plaice Pogge Pollack Poor cod River lamprey Roach Rock cook wrasse Rock goby Rudd Salmon Sand goby Sand smelt Sand sole Sea trout Shanny Short-spined sea scorpion Smelt Smooth hound Snake pipefish Sprat Stone loach Striped red mullet Thick-lipped grey mullet Thin-lipped grey mullet

HOM BNW BIB BLG BLL DGN POK COD CDT GMG SSL SOL COE CWG CUW DAB FDC DPF ELE ESB SSS FVR FLE SBG MGN GDY GPF GSE GUG FGN BTF HAD HER LAS TSE LSD WEL PLA SSN LUM MAC FMW NPF TNS PTG FPE FPI PLE POG POL POD LAR FRO SMW RKG FRD SAL SDG SMT SOS TRS SHY BRT SME SMH SKP SPR FTL MUR MTL MTN

MS MS MM ES MM MS MS MM MS ES ES MM MM MM MS MM FM ES DI MM ES MM MM MM MM MS ES MS MM FS MM MS MM FS ES MS MS MS MM MM MS FS ES FS MS FS FS MM MM MM MM DI FS MS ES FS DI ES MM MM DI MS MM DI MS MM MM FS MM MM MM

PV ZB ZB ZB PV ZB PV PV ZB ZB ZB ZB PV ZB ZB ZB ZB ZP ZB PV ZP ZB ZB ZB DV ZB ZP ZP ZB ZB ZB PV ZP DV ZP ZB ZB ZB ZB ZP ZP ZP ZP ZB ZB PV PV ZB ZB PV ZB PV OV ZB ZB OV ZB ZB ZP ZB ZB ZB PV PV ZB ZP ZP ZB ZB DV DV

16 30 24 27 22 11 30 73 16 68 5 16 24 41 5 22 8 22 81 27 78 95 100 3 14 5 43 19 3 3 38 8 11 3 62 30 3 3 76 5 5 19 22 5 16 14 5 86 35 86 30 14 14 3 14 5 32 86 68 3 70 8 35 14 3 14 76 5 3 65 8

100 51 100 6 96 86 100 100 97 4 NA 99 100 63 33 98 93 21 7 97 66 33 98 100 100 57 100 15 100 100 92 100 100 100 96 12 100 100 5 100 100 85 31 75 4 94 100 100 NA 100 81 100 88 20 0 50 99 80 26 100 31 40 66 33 100 NA 95 33 100 98 67 (continued on next page)

8

L. Connor, D. Ryan, R. Feeney et al. / Regional Studies in Marine Science 32 (2019) 100836

Table 5 (continued). Species

Common name

ID

Functional guild

Feeding guild

Raja clavata Gaidropsarus vulgaris Gasterosteus aculeatus Chelidonichthys lucernus Psetta maxima Alosa fallax Gobiusculus flavescens Merlangius merlangus Nerophis lumbriciformis

Thornback ray Three-bearded rockling Three-spined stickleback Tub gurnard Turbot Twaite shad Two-spotted goby Whiting Worm pipefish

THR TBR TSS TUB TUR TAS TSG WHG WPF

MM MS FM MM MM DI MS MM ES

ZB ZB ZP ZB PV ZP ZB PV ZP

Where : αi ∼ N(0, σ 2 site )

εj ∼ N(0, σ 2 year ) 2.4.3. Relative abundance: Functional groups The species were assigned to functional and feeding guilds as described by Elliott et al. (2007) and Potter et al. (2013); the guilds used in this study are those applied to Irish estuarine fish species by the Estuarine Multi-metric Fish Index (EMFI) (Harrison and Kelly, 2013) for assigning the ecological status of fishes in transitional waterbodies as required by the WFD. Species data were grouped according to estuarine function, and the relative abundance of each functional group captured within each estuary was calculated. The functional guilds comprise:

• diadromous species (DI), which includes both anadromous

•

•

•

•

•

and catadromous species that migrate through estuaries as part of their lifecycle to reach spawning or feeding grounds; estuarine species (ES), which includes both those species that preferentially inhabit estuaries for their entire life cycle and those species that have larval forms that live outside estuaries but that migrate back to estuaries to complete their lifecycle; freshwater migrants (FM), which are freshwater species that inhabit estuaries for part of their life cycle before returning to a freshwater habitat; freshwater stragglers (FS), which are stenohaline species that typically inhabit freshwater but that occasionally stray into the upper reaches of estuaries adventitiously; marine migrants (MM), which are marine species that inhabit estuaries for part of their life cycle before returning to a marine habitat; and marine stragglers (MS), which are stenohaline species that typically inhabit coastal waters but that occasionally stray into the lower reaches of estuaries adventitiously.

The feeding guilds comprise of:

• zoobenthivores

• • • •

(ZB), feeding predominantly on invertebrates associated with the substratum, including animals that live just above the sediment, on the sediment or in the sediment; piscivores (PV), feeding predominantly on finfish but may include large nektonic invertebrates; zooplanktivores (ZP), feeding predominantly on zooplankton; detritivores (DV), feeding predominantly on detritus and/or microphytobenthos; omnivores (OV), feeding predominantly on filamentous algae, macrophytes, periphyton, epifauna and infauna.

The vast majority of all captures throughout the sampling programme consisted of two functional groups, i.e. marine migrants and estuarine species (Tables 4 & 5), so only these groups were included for further analysis. Generalised Linear Mixed Effect Models (GLMM) with a binomial distribution for proportion data (Zuur et al., 2007) were

% occurrence 5 14 62 5 11 3 57 57 8

% juveniles 75 46 54 100 100 100 99 99 0

fitted. As for species richness, fyke nets and seine nets were considered separately, with a duplicate modelling process for each gear. A weighting function was also added to the model to account for differences in total capture counts between sampling surveys. Preliminary analyses of the models showed overdispersion, so an observation level random effect (OLRE) was added to the model (Harrison, 2015). Model selection and goodness of fit estimation was carried out using the same explanatory variables (Table 3) and methods as described above. The response variables that made up the vast majority of all captures were marine migrant-seine, marine migrant-fyke and estuarine species-seine, and separate models were specified for each of these. Functional group proportionijk ∼ Binomial(ηijk ) Logit(ηijk ) = β1 + β2 X Latitudeijk + β3 X Estuary mouth widthijk

+ β4 X MouthWidth:Areaijk + β5 X Estuary areaijk + β6 X Fetch indexijk + β7 X Subtidal areaijk + αi + εj + νk Where: αi ∼ N(0, σ 2 site )

εj ∼ N(0, σ 2 year ) νk ∼ N(0, σ 2 OLRE ) Assumptions of all final models were verified by visual assessment of normality and homoscedasticity of model residuals. All statistical analyses and model visualisations were performed in R (R Core Team, 2017; Wickham, 2009). Main effects with a p level <0.05 were considered as ecologically relevant. 2.4.4. Species ordinations Relative abundances of functional groups were calculated for each estuary and year to explore patterns of functional traits in fish communities between estuary groupings. As above, data for fyke and seine nets were analysed separately. First, estuaries were grouped by hierarchical clustering according to similarities between species or functional group composition using the function ‘‘hclust’’ in the R package ‘‘vegan’’ (Oksanen, 2015). The data were then plotted using non-metric multidimensional scaling (nMDS), using Bray–Curtis dissimilarity indices as the input matrix for each ordination. Each nMDS was carried out using the function ‘‘metaMDS’’ (Oksanen, 2015), where all data were scaled and centred prior to ordination. This ordination technique also allowed spatial visualisation of the estuary groups which were defined by hierarchical clustering. Finally, important estuary predictor variables were projected onto the ordination plots as a vector using the function ‘‘envfit’’ (Oksanen, 2015), where the arrow points in the direction of most rapid change for each estuary variable. 3. Results The total sample consisted of species captured in beach seines 65 species captured in fyke nets. of 202,917 individual fish of 80

190,648 individual fish of 68 and 12,269 individual fish of In total, the sample consisted species. Juveniles made up a

L. Connor, D. Ryan, R. Feeney et al. / Regional Studies in Marine Science 32 (2019) 100836

large proportion of the population (mean percentage of juveniles = 73%), with 57 out of 77 species consisting of <50% juveniles (Table 5). Several species are well distributed in Irish coastal waters (Went, 1978). Species that are common in most temperate estuaries were commonly recorded during the current study. Flounder, five-bearded rockling, plaice, pollack, sand goby (Pomatoschistus minutus), European eel, fifteen-spined stickleback (Spinachia spinachia), sprat, long-spined sea scorpion (Taurulus bubalis) and cod were the ten most widespread fish species (Table 5). Flounder was encountered in all waterbodies. Five-bearded rockling were found in 90% of sites surveyed, pollack and sand goby (87% of sites), plaice (85% of sites) and European eel (82% of sites). Twenty-seven species were encountered in less than 10% of estuaries, and many of these were marine migrants or marine stragglers, such as cuckoo wrasse (Labrus mixtus), rock cook wrasse (Centrolabrus exoletus), striped red mullet (Mullus surmuletus), thin-lipped grey mullet (Chelon ramada), thornback ray (Raja clavata), gilthead bream (Sparus aurata), sand sole (Solea lascaris), smooth hound (Mustelus mustelus) and grey gurnard (Eutriglia gurnardus) (Table 5). Apart from commercially important species such as cod and herring being encountered, a number of important species listed under the Habitats Directive were also recorded such as twaite shad (Alosa fallax), European smelt (Osmerus eperlanus), Atlantic salmon and brown trout/sea trout (King et al., 2011). Some of these species are also of angling interest. Marine migrants were the most diverse functional guild present with 33 species, followed by 19 marine stragglers, 11 estuarine species, nine freshwater stragglers, six diadromous species and two freshwater migrant species (Table 5). Length frequency analysis indicated that 87% of marine migrant individuals and 57% of estuarine species individuals captured were juvenile fish. Five feeding guilds were recorded in the estuaries, of these zoobenthivores were the most common group (43 species) followed by 16 zooplanktivore species, 15 piscivores, 4 detritivores and 2 omnivores (Table 5). 3.1. Species richness 3.1.1. Shallow littoral habitat A total of 190,648 fish which included 68 different species were caught in seine nets across all estuaries and years covered in this study. Species richness varied greatly (mean 13.1, maximum 33 and minimum 3) between estuary samples. The highest mean species richness across all survey years was 29 species in the Shannon Estuary (Fig. 2). The best fitting linear model included three estuary variables (marginal R2 = 0.54; conditional R2 = 0.58). Estuaries in higher latitudes had lower species richness overall. Increasing MouthWidth:Area was also associated with decreasing species richness. Higher species richness was evident in larger estuaries (Table 6, Fig. 3). 3.1.2. Subtidal habitat A total of 12,269 fish of 65 different species were caught in fyke nets across all estuaries and years covered in this study. Across all estuaries and years, the maximum species richness recorded through fyke netting was 27, mean was 10.4, and the minimum was 3. The highest mean species richness across all survey years was 25.67 species in the Shannon Estuary (Fig. 4). The best fitting linear model included four estuary variables (marginal R2 = 0.56; conditional R2 = 0.58) and all four significantly affected species richness (Table 7). As with sampling in the shallow littoral, large estuaries were associated with higher

9

Table 6 The generalised linear mixed-effects model output for the response variable species richness (seine netting) fitted by maximum likelihood. Variables are described in Table 2, all variables were centred and scaled. Intercept Latitude MouthWidth:Area Estuary area

Coefficient

SE

2.5362 −0.14847 −0.16162 0.16716

0.05239 0.04165 0.04826 0.03439

z value 48.41 −3.56 −3.35 4.86

P value

<0.0001 <0.0005 <0.001 <0.0001

Table 7 The generalised linear mixed-effects model output for the response variable species richness (fyke netting) fitted by maximum likelihood. Variables are described in Table 2, all variables have been centred and scaled. (Intercept) Estuary mouth width MouthWidth:Area Estuary area % subtidal

Coefficient

SE

2.27629 0.19189 −0.2436 0.10433 0.16591

0.0506 0.04854 0.06358 0.04112 0.04761

z value 44.99 3.95 −3.83 2.54 3.48

P value

<0.0001 <0.0001 <0.0005 <0.05 <0.0005

Table 8 The generalised linear mixed-effects model (binomial) output for the response variable marine migrant relative abundance (seine netting) fitted by maximum likelihood. Variables are described in Table 2, all variables have been centred and scaled. (Intercept) Estuary area

Coefficient

SE

z value

P value

−0.8519

0.2890 0.2660

−2.948

<0.005 <0.01

0.7444

2.798

species richness and increasing MouthWidth:Area was associated with decreasing species richness. The survey data also found that the greater the proportion of subtidal habitat in an estuary, the greater the species richness. Increasing estuary mouth width was found to be related to a significant increase in species richness (Fig. 5). 3.2. Relative abundance: Functional groups — marine migrants 3.2.1. Shallow littoral habitat Marine migrants were present in all but one estuary during sampling of the shallow littoral areas. On average, this functional group comprised of 35.5% of all seine net captures (Table 4, Fig. 6). The best fitting model included a single variable. Marine migrant relative abundance was positively related to estuary area (Table 8, Fig. 7). However, most of the data’s variance was not explained by the model coefficients (marginal R2 = 0.08; conditional R2 = 0.56). 3.2.2. Subtidal habitat Marine migrants were present in all estuaries during sampling of the subtidal areas (Fig. 6). This functional group contained the largest proportion of all fyke net captures, with an average of 77% (Table 4, Fig. 8). The best fitting model included two estuary variables. There was a weak negative relationship between marine migrants and the proportion of subtidal habitat. In contrast, there was a weak positive relationship between marine migrants and MouthWidth:Area (Table 9, Fig. 8). Most of the data’s variance was not explained by the model coefficients (marginal R2 = 0.04; conditional R2 = 0.24). 3.3. Relative abundance: Functional groups — estuarine species 3.3.1. Shallow littoral habitat Estuarine species were ubiquitous during sampling of the shallow littoral habitats of the study estuaries (Fig. 9). On average,

10

L. Connor, D. Ryan, R. Feeney et al. / Regional Studies in Marine Science 32 (2019) 100836

Table 9 The generalised linear mixed-effects model (binomial) output for the response variable marine migrant relative abundance (fyke netting) fitted by maximum likelihood. Variables are described in Table 2, all variables have been centred and scaled. (Intercept) SubtidalArea MouthWidth:Area

Coefficient

SE

1.4766 −0.3237 0.3258

0.1377 0.1486 0.1478

z value 10.721 −2.179 2.205

P value

<0.0001 <0.05 <0.05

Table 10 The generalised linear mixed-effects model (binomial) output for the response variable estuarine species relative abundance (seine netting) fitted by maximum likelihood. Variables are described in Table 2; all variables have been centred and scaled. (Intercept) % subtidal MouthWidth:Area Estuary mouth width

Coefficient

SE

z value

−0.1251 −0.8466

0.2162 0.2269 0.2396 0.2255

−0.579 −3.731

0.5137

−0.6757

2.144

−2.996

P value 0.56272

<0.0005 <0.05 <0.005

this functional group comprised of 48% of all seine net captures (Table 4). The best-fitting model included three estuary variables (Table 10). Two variables showed a negative relationship with relative abundance of estuarine species (% subtidal and mouth width) (Fig. 10), while increasing MouthWidth:Area had a minor positive relationship with the proportion of estuarine species captured in the shallow littoral. A large proportion of the data’s variance was not explained by the model coefficients (marginal R2 = 0.17; conditional R2 = 0.53). 3.4. Multivariate analyses 3.4.1. Relative abundance – functional groups – shallow littoral habitat The nMDS ordination showed that two major estuary groups (as defined by hierarchical clustering) located on the bottom left and right of the ordination, were defined by greater marine migrant (MM) and estuarine species (ES) abundance, respectively. The largest cluster group represented sites with a more even mix of functional groups. This group is located in the lower centre of the ordination (DI) (Fig. 11). The final two clustering groups,

Fig. 6. Mean abundance of marine migrants for all years surveyed.

located in the upper half of the ordination plot, are associated with freshwater migrants (FM) and marine stragglers (MS) which consisted of only 8.7% and 4.3% of total catch, respectively (Fig. 11, Table 11). 3.4.2. Relative abundance – functional groups – subtidal habitat The nMDS ordination showed that the functional group composition of most estuaries in the subtidal habitat is quite closely related, driven largely by the proportion of marine migrants (MM) (Fig. 12). Estuary groups away from the main cluster are characterised by the functional groups MS, ES, FM and DI. These were generally caught at low proportions during fyke netting (Table 4). Observing the superimposed environmental vector on

Table 11 Hierarchical clustering of all estuaries (and survey years). Grouped according to functional group composition of fish species in the shallow littoral - seine netting. Group 1

Group 2

Group 3

Group 4

Group 5

Argideen Estuary (2008) Avoca Estuary (2015) Ballysadare Estuary (2008) Ballysadare Estuary (2015) Bandon Estuary (2009) Barrow Nore Suir Estuary (2010) Barrow Nore Suir Estuary (2013) Barrow Nore Suir Estuary (2016) Bridgetown Estuary (2009) Broad Lough (2008) Broad Lough (2010) Castlemaine Harbour (2015) Garavoge Estuary (2008) Ilen Estuary (2008) Inner Donegal Bay (2009) Kinvarra Bay (2009) Kinvarra Bay (2015) Munster Blackwater Estuary (2008) Owenacurra Estuary (2008) Owenacurra Estuary (2010) Rogerstown Estuary (2008) Shannon Estuary (2017) Swilly Estuary (2009)

Argideen Estuary (2017) Bandon Estuary (2016) Boyne Estuary (2012) Boyne Estuary (2015) Corrib Estuary (2008) Dublin Harbour (2008) Dungarvan Harbour (2008) Erne Estuary (2009) Erne Estuary (2012) Erne Estuary (2015) Erriff Estuary (2008) Gweebarra Estuary (2009) Gweebarra Estuary (2012) Lee K Estuary (2008) Rogerstown Estuary (2010) Sruwaddacon Bay (2008) Tullaghan Bay (2008)

Avoca Estuary (2008) Avoca Estuary (2010) Boyne Estuary (2009) Castlemaine Harbour (2011) Dublin Harbour (2010) Dundalk Bay (2009) Gweebarra Estuary (2015) Lough Mahon Estuary (2008) Lough Mahon Estuary (2010) Shannon Estuary (2008) Shannon Estuary (2014) Slaney Estuary (2014)

Camus Bay (2008) Camus Bay (2009) Camus Bay (2015) Feale Estuary (2008) Moy Estuary (2008) Newport Bay (2008) Slaney Estuary (2009)

Inner Kenmare River (2010) Kilmakilloge Harbour (2008) Westport Bay (2008)

L. Connor, D. Ryan, R. Feeney et al. / Regional Studies in Marine Science 32 (2019) 100836

11

Fig. 7. Relationship between relative abundance of the functional group marine migrants and estuary area in the shallow littoral zone of Irish estuaries. Only statistically significant regressions are presented. Each sample (n = 62) represents marine migrant relative abundance calculated from beach seine data, in an estuary in a particular year (2008–2016).

Fig. 9. Mean abundance of estuarine species for all years surveyed.

Fig. 8. Relationship between relative abundance of the functional group marine migrants and selected environmental variables in the subtidal zone of Irish estuaries. Only statistically significant regressions are presented. Each sample (n = 62) represents marine migrant relative abundance calculated from fyke net data, in an estuary in a particular year (2008–2016).

the ordination plot, it is clear that any correlation between estuary functional group composition ordination and environmental variables is low (Fig. 12). 4. Discussion In this study, marine predators are well represented by the marine migrant and estuarine species guilds, which made up most of the individuals and species captured. Migratory groups were represented by the six species that made up the diadromous guild analysed in this study, which included European eel and European smelt. With 19 species recorded in this study, the marine straggler guild is well represented throughout Irish estuaries in terms of number of species. Occurring only in low numbers in estuaries, this guild typically inhabits more saline areas (Elliott et al., 2007), and species present in Irish estuaries mostly consist of a range of wrasses, gobies, and dogfish. Some

Fig. 10. Relationship between relative abundance of the functional group estuarine species and selected environmental variables in the shallow littoral zone of Irish estuaries. Only statistically significant regressions are presented. Each sample (n = 62) represents estuarine species relative abundance calculated from beach seine data, in an estuary in a particular year (2008–2016).

marine predators such as sea bass are well equipped to cope with reduced salinity and frequently penetrate the estuaries in

12

L. Connor, D. Ryan, R. Feeney et al. / Regional Studies in Marine Science 32 (2019) 100836

Fig. 11. Two-dimensional nMDS plot showing the relative abundance of five functional groups (FM — freshwater migrants, MS — marine stragglers, FS — freshwater stragglers, ES — estuarine species, DI — diadromous species, MM — marine migrants) in the shallow littoral zone across all estuaries. Arrow vectors (fit by envfit; vegan) point in the direction of the most rapid change in environmental variable. Length of arrow is proportional to the correlation between the environmental variable and ordination (SA; Subtidal area, MW; Mouth width, EA; Estuary area). Each point (n = 62) denotes an estuary in a particular year (2008–2016). Estuaries grouped by hierarchical clustering. Solid line = Group1, dashed = Group2, dotted = Group3, dotdash = Group4, long dash = Group5. For grouping details refer to Table 10. Stress = 0.1.

Fig. 12. Two dimensional nMDS plot showing the relative abundance of five functional groups (FM — freshwater migrants, MS — marine stragglers, FS — freshwater stragglers, ES — estuarine species, DI — diadromous species, MM — marine migrants) in the subtidal zone across all estuaries. Arrow vectors (fit by envfit; vegan) point in the direction of the most rapid change in environmental variable. Length of arrow is proportional to the correlation between the environmental variable and ordination (MW.EA; Mouth width:Area, MW; Mouth width). Each point (n = 62) denotes an estuary in a particular year (2008–2016). Estuaries grouped by hierarchical clustering. Solid line = Group1, dashed = Group2, dotted = Group3, dotdash = Group4, long dash = Group5. Stress = 0.04.

search of food, (Pickett et al., 2002; Pawson et al., 2007). It is confirmed here that although estuaries are not core reproductive and feeding habitat for marine migrants, this guild is the most diverse and relatively most abundant component of the estuarine fish community in Ireland, which reflects the tendency of some marine migrant species to enter estuaries in large numbers in the juvenile phase of their life cycle (Elliott et al., 2007). Nonetheless, estuarine species comprised of the most relatively abundant component of the shallow littoral zone. In contrast, the constantly changing nature of estuaries, with their tidal regimes and salinity gradients from freshwater to fully marine conditions, is a challenging environment for freshwater fish to survive in, and the presence of only nine species of freshwater stragglers in Irish estuaries recorded in this study reflects this. By definition,

freshwater stragglers are found almost accidentally in estuaries, due to large freshwater inflows or flooding (Elliott et al., 2007). The main driver of the ordination plots for Irish estuaries is changing proportion of estuarine species versus marine migrants in the shallow littoral and subtidal habitats. Most fish caught in the subtidal habitat were marine migrants (77%). Although there are some small clusters of estuaries driven by changes in functional group composition, the subtidal habitat of Irish estuaries consists largely of marine migrant species. The current results showed a clear trend in species type and functional guild as estuaries became larger and more open. The results show a large group of estuaries where marine migrants consistently dominated the fish population, and environmental vectors indicate that this is a result of increasing estuary mouth width and estuary area. As estuary area increased, the proportion of marine migrants in the shallow littoral increased, confirming the importance of marine migrants in contributing to overall fish species community composition in estuaries. Moreover, increasing estuary mouth width is related to a decreasing proportion of estuarine species. Although goodness-of-fit tests found that the models used to examine changes in functional group proportions between estuaries could not explain much of the variance, some significant trends emerged. The results indicate that in larger estuaries which are more open to the sea, marine migrants are more likely to replace estuarine species in the shallow littoral areas. This trend is likely to be even more pronounced in estuaries that have a greater proportion of its substrate remaining underwater throughout the tidal cycle i.e. subtidal habitat. The estuarine species guild depends on estuaries for feeding and reproductive habitat, and the abundance of this guild in the shallow littoral zone highlights the vital nursery function that Irish estuaries perform for this group of fish. The negative relationship between estuarine species and the percentage of subtidal area in estuaries studied, as well as the preponderance of estuarine species in the shallow littoral habitat, reflects the reliance of this guild on the range of habitats within estuaries that they utilise throughout their lifecycle. The importance of estuaries as nursery habitat is further supported by the fact that the marine migrant and estuarine species guilds consisted of 87% and 57% juveniles respectively. For this study, fish species richness is positively correlated to estuary area in both shallow littoral and subtidal habitats which is consistent with other studies that highlight estuary area as a significant predictor of taxonomic richness in studies of US (Horn and Allen, 1976; Monaco et al., 1992), Australian (Pease, 1999), South African (Harrison and Whitfield, 2006b), South American (Araújo and Costa de Azevedo, 2001), European (Franco et al., 2008; Nicolas et al., 2010) and Irish estuaries (Harrison et al., 2017; Harrison and Kelly, 2013). Species–area relationships are a well-attested phenomenon in ecological communities, including estuarine fish. Area has been underlined as a highly significant structuring effect for European estuary fish assemblages (Elliott and Dewailly, 1995). On the basis of generalised linear models, Nicolas et al. (2010) concluded that estuarine system size, together with estuary river mouth entrance width and distance to the continental shelf width, were the best explanatory variables of estuarine fish species richness at a large scale. In their study of predictors of species richness from global to local spatial extents, Vasconcelos et al. (2015) concluded that the processes that influence estuarine fish community structure are spatially hierarchical: processes that influence connectivity with and colonisation from marine habitat are important at large regional spatial extents, but these give way to species–area relationships and availability of habitat at more local scales. A larger estuary is more likely to contain more diverse habitats than a smaller one and

L. Connor, D. Ryan, R. Feeney et al. / Regional Studies in Marine Science 32 (2019) 100836

to offer a larger habitat area, and therefore, a higher carrying capacity. Large estuaries also have a complete salinity gradient from tidal freshwater to euryhaline area. Small estuaries with a low river input tend to fill with marine water only during high tide, without a real mixing zone of brackish water. This difference supports the assumption that larger estuaries contain more diverse habitats and species than smaller ones. Several variables that describe the physical shape of estuaries and their connectivity to adjoining coastal waters were calculated to explore the influence of the estuarine seascape on fish community structure, but most of these were rejected for further analysis during preliminary data exploration due to covariance with other variables. One retained variable, (MouthWidth:Area ratio) was found to exert a strong negative effect on species richness in both the subtidal and littoral habitat. This contrasts with the positive effect of both estuary mouth width and estuary area on species richness. This finding may indicate that accessibility between estuarine habitat and adjoining coastal waters is constrained by the nature of the boundary between them and the physical configuration of the estuary. Estuaries with a low MouthWidth:Area ratio tend to be relatively large compared with their coastal mouth width; this effect scales across different sized estuaries, but this may be especially driven by large estuaries. This is an initial attempt to explain this phenomenon and warrants the further exploration of the physical and hydrographic characteristics of estuaries, including depths, tidal regimes and other factors. The spatial distribution of species richness along environmental gradients could better elucidate the potential impact of such factors on fish assemblages and the connectivity of estuarine habitat. Salinity, temperature and openness to the sea are frequently identified as the key environmental components of estuarine typology that drive structuring of fish communities at the biogeographical scale (Harrison, 2002, 2003; Harrison et al., 2017; Harrison and Whitfield, 2006c; Nicolas et al., 2010; Vasconcelos et al., 2015). Greater connectivity of estuaries with the marine ecosystem and larger estuary area positively influence species richness (Henriques et al., 2017). In this study, latitude and estuary mouth width were used as proxies for temperature and marine connectivity, respectively, were confirmed to have a role in structuring fish communities Irish estuaries. Estuaries at higher latitudes in Ireland tended to have lower species richness in the shallow littoral zone, possibly because species which have a more southerly distribution in warmer waters, such as mullet and bass, do not move so far north into cooler waters to colonise estuaries. Conversely, openness to the sea, as indicated by estuary mouth width, was positively associated with species richness in the shallow littoral zone. Partitioning the guilds between habitat types in this study showed that these effects are due to the relative abundance of marine migrants, highlighting the role that colonisation by marine species plays in augmenting the species richness of estuaries at local and regional biogeographic scales. In estuaries and marine habitats, changes in fish communities will continue as fish change their distributions relative to environmental preferences, including temperature. This shift may lead to the loss of some cold-water adapted species that are important for recreational angling and commercial harvesting, such as cod and herring, from some areas around Britain and Ireland, and the increase of warm-water adapted species (FSBI, 2007), such as sea bass, gilthead bream and golden-grey mullet. Shifts in the distribution patterns of marine fish species off Ireland have been documented, with an increase in the occurrence of Lusitanian, or warmer water, species, such as John Dory, striped red mullet, pilchard, boarfish, anchovy, poor cod and lesser-spotted dogfish (Nolan et al., 2010). These ongoing regime shifts in biogeographical distribution of fish species in the North Atlantic can be expected to have consequences for fish species distribution

13

and community guild structure in Irish estuaries; the results of this study provide baseline data on the distribution in estuaries around Ireland of several species, such as flounder, cod, poor cod, lesser spotted dogfish, snake pipefish, lesser sandeel, and striped red mullet, that have been identified as bioclimatic indicators of marine fish assemblages and their response to changes in sea temperatures (Heath et al., 2012; Nolan et al., 2010; Rijnsdorp et al., 2010). In conclusion, estuaries are important for fish biodiversity through their multiple functions as spawning, nursery, feeding and shelter areas for a range of fish species using the waters as residents, as seasonal or juvenile visitors or simply passing between the truly marine and the freshwater habitats. The current study provides a baseline showing the biogeography and fish community structure in Irish estuaries and how it is related to ecosystem characteristics and environmental variables. The value of the current eleven years of estuarine fish community dataset is substantial. Not only does it provide a time stamped baseline for monitoring future climate change impacts and an important reference point WFD and Habitats Directive reporting to the EU, but it also gives an indication of the use of the estuaries by different fish groups of recreational, commercial and conservation importance. Acknowledgements This study was supported by Inland Fisheries Ireland. The authors would like to gratefully acknowledge the invaluable assistance given by Inland Fisheries Ireland staff during the project. References Araújo, F.G., Costa de Azevedo, M.C., 2001. Assemblages of southeast-south Brazilian coastal systems based on the distribution of fishes. Estuar. Coast. Shelf Sci. 52 (6), 729–738. http://dx.doi.org/10.1006/ecss.2001.0778. Araújo, F.G., Bailey, R.G., Williams, W.P., 1998. Seasonal and between-year variations of fish populations in the middle Thames estuary: 1980–1989. Fish. Manage. Ecol. 5 (1), 1–21. http://dx.doi.org/10.1046/j.1365-2400.1998. 00088.x. Araújo, F.G., Williams, W.P., Bailey, R.G., Araujo, F.G., 2000. Fish assemblages as indicators of water quality in the middle Thames estuary, England (1980-1989). Estuaries 23 (3), 305. Arnold, T.W., 2010. Uninformative parameters and model selection using Akaike’s Information Criterion. J. Wildlife Manage. 74 (6), 1175–1178. Bamber, R., 2010. Coastal saline lagoons and the Water Framework Directive. Natural England Commissioned Report NECR039. www.naturalengl{and}.org. uk. Barton, K., 2018. MuMIn: multi-model inference. R Package 1.42.1. https://CRAN. Rproject.org/package=MuMIn. Bates, D., Mächler, M., Bolker, B., Walker, S., 2015. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67 (1), 1–48. http://dx.doi.org/10.18637/ jss.v067.i01. Breine, J., Maes J. Ollevier, F., Stevens, M., 2011. Fish assemblages across a salinity gradient in the Zeeschelde estuary (Belgium). Belg. J. Zool. 141 (2), 21–44. Burnham, K.P., Anderson, D.R., 2002. Model Selection and Multimodel Inference. Springer New York, New York, NY, http://dx.doi.org/10.1007/b97636. Burrows, M.T., Harvey, R., Robb, L., 2008. Wave exposure indices from digital coastlines and the prediction of rocky shore community structure. Mar. Ecol. Progr. Ser. 353, 1–12. Cabral, H.N., 2000. Distribution and abundance patterns of flatfishes in the sado estuary, Portugal. Estuaries 23 (3), 351. Cabral, H., Costa, M.J., 2001. Abundance, feeding ecology and growth of 0-group sea bass, Dicentrarchus labrax, within the nursery areas of the Tagus estuary. J. Mar. Biol. Assoc. U.K. 81 (4), 679–682, https://www.cambridge.org/core/article/abundance-feeding-ecology-andgrowth-of-0group-sea-bass-dicentrarchus-labrax-within-the-nurseryareas-of-the-tagus-estuary/184514AE0FBABC2A949861DC68427F25. CEN, 2005. Water Quality - Guidance on the scope and selection of fish sampling methods; European Committee for Standarization. CEN EN 14962. Claridge, P.N., Potter, C.E., 1983. Movements, abundance, age composition and growth of bass, Dicentrarchus labrax, in the Severn Estuary and inner Bristol channel. J. Mar. Biol. Assoc. U.K 63, 871–879.

14

L. Connor, D. Ryan, R. Feeney et al. / Regional Studies in Marine Science 32 (2019) 100836

Claridge, P.N., Potter, I.C., 1984. Abundance, movements and size of gadoids (Teleostei) in the Severn Estuary. J. Mar. Biol. Assoc. U.K 64 (4), 771–790, https://www.cambridge.org/core/article/abundancemovements-and-size-of-gadoids-teleostei-in-the-severn-estuary/ 1E37956F5CB8F0324B810C695382C1D5. Claridge, P.N., Potter, I.C., 1985. Distribution, abundance and size composition of mullet populations in the Severn Estuary and Bristol Channel. J. Mar. Biol. Assoc. U.K 65 (2), 325–335, https: //www.cambridge.org/core/article/distribution-abundance-and-sizecomposition-of-mullet-populations-in-the-severn-estuary-and-bristolchannel/E040CBB3C2AA86710465316D44FBB3AB. Claridge, P.N., Potter, I.C., 1987. Size composition and seasonal changes in abundance of juvenile sole, Solea solea, in the Severn Estuary and Inner Bristol Channel. J. Mar. Biol. Assoc. U.K 67 (3), 561–569, https://www.cambridge.org/core/article/size-composition-and-seasonalchanges-in-abundance-of-juvenile-sole-solea-solea-in-the-severn-estuaryand-inner-bristol-channel/FD340DA9A792E041F41D98AB1A1DB6D2. Coates, S., Waugh, A., Anwar, A., Robson, M., 2007. Efficacy of a multi-metric fish index as an analysis tool for the transitional fish component of the Water Framework Directive. Mar. Pollut. Bull. 55. EC, 2019. http://ec.europa.eu/environment/water/waterframework/facts_figures/ guidance_docs_en.htm. Elliott, M., Dewailly, F., 1995. The structure and components of European estuarine fish assemblages. Neth. J. Aquat. Ecol. 29 (3), 397–417. http: //dx.doi.org/10.1007/BF02084239. Elliott, M., Taylor, C.J.L., 1989. The structure and functioning of an estuarine/marine fish community in the Forth Estuary, Scotland. In: Proceedings of the 21st European Marine Biology Symposium, Gdansk; pp. 227-240. Elliott, M., Whitfield, A.K., Potter, I.C., Blaber, S.J.M., Cyrus, D.P., Nordlie, F.G., et al., 2007. The guild approach to categorizing estuarine fish assemblages: A global review. Fish Fish. 8, 241–268. EPA, 2005. The Characterisation and analysis of Ireland’s river basin districts in accordance with Section 7 (2 & 3) of the European Communities (Water Policy) Regulations 2003 (SI 722 of 2003). National Summary Report (Ireland): Environmental Protection Agency. EPA, 2006. Water Framework Directive Monitoring Programme: Environmental Protection Agency, Ireland. Fish, J.D., 1989. A Student’s Guide to the Seashore. pp. 500. Franco, A., Elliott, M., Franzoi, P., Torricelli, P., 2008. Life strategies of fishes in European estuaries: The functional guild approach. Mar. Ecol. Progr. Ser. 354, 219–228. Froese, R. and Pauly, D. (Eds), 2018. FishBase. World Wide Web electronic publication. www.fishbase.org (10/2018). FSBI, 2007. Climate change and the fishes of Britain and Ireland: Briefing Paper 4. Cambridge, UK: Fisheries Society of the British Isles. Gelman, A., 2008. Scaling regression inputs by dividing by two standard deviations. Stat. Med. 27 (15), 2865–2873. http://dx.doi.org/10.1002/sim. 3107. Greenwood, M.F.D., Hill, A.S., McLusky, D.S., 2002. Trends in abundance of benthic and demersal fish populations of the lower Forth Estuary, East Scotland, from 1982–2001. J. Fish Biol. 61 (sA), 90–104. http://dx.doi.org/ 10.1111/j.1095-8649.2002.tb01764.x. Haedrich, R.L., 1987. Estuarine fishes. In: Ketchum, B. (Ed.), Ecosystems of the World, 26. Estuarine and Enclosed Seas. Elsevier, Amsterdam, pp. 183–207, Ch. 7. Harborne, A.R., Mumby, P.J., ZŻychaluk, K., Hedley, J.D., Blackwell, P.G., 2006. Modeling the beta diversity of coral reefs. Ecology 87 (11), 2871–2881. http://dx.doi.org/10.1890/0012-9658(2006)87%5b2871:MTBDOC%5d2.0.CO;2. Harrison, T.D., 2002. Preliminary assessment of the biogeography of fishes in South African estuaries. Mar. Freshw. Res. 53, 479–490. Harrison, T.D., 2003. Biogeography and community structure of fishes in South African estuaries (PhD). Harrison, X.A., 2015. A comparison of observation-level random effect and BetaBinomial models for modelling overdispersion in binomial data in ecology & evolution. PeerJ 3, e1114. http://dx.doi.org/10.7717/peerj.1114. Harrison, T.D., Armour, N.D., McNeill, M.T., Moorehead, P.W., 2017. A comparative study of Northern Ireland’s estuaries based on the results of beam trawl fish surveys. Estuar. Coast. Shelf Sci. 198, 172–182, http://www.sciencedirect. com/science/article/pii/S0272771417305395. Harrison, T.D., Kelly, F., 2013. Development of an estuarine multi-metric fish index and its application to Irish transitional waters. Ecol. Indic. 34, 494–506. Harrison, T.D., Whitfield, A.K., 2006a. Application of a multimetric fish index to assess the environmental condition of South African estuaries. Estuaries Coasts 29 (6B), 1108–1120. Harrison, T.D., Whitfield, A.K., 2006b. Estuarine typology and the structuring of fish communities in South Africa. Environ. Biol. Fishes 75, 269–293. Harrison, D.T., Whitfield, A.K., 2006c. Temperature and salinity as primary determinants influencing the biogeography of fishes in South African estuaries estuarine. Coast. Shelf Sci. 66, 335–345.

Heath, M.R., Neat, F.C., Pinnegar, J.K., Reid, D.G., Sims, D.W., Wright, P.J., 2012. Review of climate change impacts on marine fish and shellfish around the UK and Ireland. Aquat. Conserv.-Mar. Freshw. Ecosyst. 22 (3), 337–367. http://dx.doi.org/10.1002/aqc.2244. Heessen, H.J., Daan, N., Ellis, J.R. (Eds.), 2015. Fish Atlas of the Celtic Sea, North Sea and Baltic Sea: Based on International Research-Vessel Surveys. Wageningen Academic Publishers, Wageningen, Netherlands. Henderson, P.A., Bird, D.J., 2010. Fish and macro-crustacean communities and their dynamics in the Severn Estuary. Mar. Pollut. Bull. 61, 100–114. Henkel, M., 2015. 21st Century Homestead. In: Sustainable Agriculture II: Farming and Natural Resources; pp. 36. Henriques, S., Guilhaumon, F., Villéger, S., Amoroso, S., França, S., Pasquaud, S., et al., 2017. Biogeographical region and environmental conditions drive functional traits of estuarine fish assemblages worldwide. Fish Fish. 18 (4), 752–771. http://dx.doi.org/10.1111/faf.12203. Horn, M.H., Allen, L.G., 1976. Numbers of species and faunal resemblance of marine fishes in California bays and estuaries. Bull. South. Calif. Acad. Sci. 75, 159–171, Bulletin Southern California Academy of Sciences 75, 159–71. IFCA, 2017. Devon and Severn Inshore Fisheries and Conservation Authority. Management of the Live Wrasse Pot Fishery. Report. Jorge, I., Monteiro, C.C., Lasserre, G., 2002. Fish community of mondego estuary: Space-temporal organization. In: Pardal, M.A., Marques, J.C., Graça, M.A. (Eds.), Aquatic Ecology of the Mondego River Basin. Global Importance of Local Experience. Imprensa da Universidade de Coimbra, Coimbra. Jovanovic, B., Longmore, C., O’Leary, Á., Mariani, S., 2007. Fish community structure and distribution in a macro-tidal inshore habitat in the Irish sea. Estuar. Coast. Shelf Sci. 75 (1), 135–142, http://www.sciencedirect.com/ science/article/pii/S0272771407001837. Kelly, F.L., Connor, L., Matson, R., Feeney, R., Morrissey, E., Coyne, J., et al., 2014. Sampling fish for the Water Framework Directive - Summary Report 2013: Internal Report: Inland Fisheries Ireland. Kelly, F.L., Connor, L., Matson, R., Feeney, R., Morrissey, E., Coyne, J., et al., 2015. Sampling Fish for the Water Framework Directive - Summary Report 2014: Internal Report: Inland Fisheries Ireland. Kelly, F.L., Connor, L., Matson, R., Feeney, R., Morrissey, E., Wogerbauer, C., et al., 2013. Sampling fish for the Water Framework Directive - Summary Report 2012: Internal Report: Inland Fisheries Ireland. Kelly, F.L., Connor, L., Matson, R., Morrissey, E., O’Callaghan, R., Wogerbauer, C., et al., 2010. Sampling fish for the Water Framework Directive - Summary Report 2009: Internal Report: The Central Fisheries Boards. Kelly, F.L., Connor, L., Wightman, G., Matson, R., Morrissey, E., O’Callaghan, R., et al., 2009. Sampling fish for the Water Framework Directive - Summary report 2008: Internal Report: Central Fisheries Boards. Kelly, F.L., Harrison, A.J., Connor, L., Matson, R., Morrissey, E., Feeney, R., et al., 2011. Sampling fish for the Water Framework Directive - Summary Report 2010: Internal Report: Inland Fisheries Ireland. Kelly, F.L., Harrison, A., Connor, L., Matson, R., Morrissey, E., Wogerbauer, C., et al., 2012. Sampling fish for the Water Framework Directive - Summary Report 2011: Internal Report: Inland Fisheries Ireland. King, J.J., Marnell, F., Kingston, N., Rosell, R., Boylan, P., Caffrey, J.M., et al., 2011. Ireland Red List No. 5: Amphibians, Reptiles and Freshwater Fish. Dublin, Ireland: National Parks and Wildlife Service, Department of Arts, Heritage and the Gaeltacht; 2009-2016. Kültz, D., 2015. Physiological mechanisms used by fish to cope with salinity stress. J. Exp. Biol. 218 (Pt 12), 1907–1914. http://dx.doi.org/10.1242/jeb. 118695. Lepage, M., Harrison, T., Breine, J., Cabral, H., Coates, S., Galván, C., García, P., Zwanette, J., Kelly, F., Mosch, E.C., Pasquaud, S., Scholle, J., Uriarte, A., Borja, A., 2016. An approach to intercalibrate ecological classification tools using fish in transitional water of the North East Atlantic. Ecol. Indic. 67, 318–327. http://dx.doi.org/10.1016/j.ecolind.2016.02.055. Malhotra, A., Fonseca, M.S., 2007. WEMo (Wave Exposure Model): Formulation, Procedures and Validation. NOAA Technical Memorandum NOS NCCOS, 65: 28 NOAA. McGarigal, K., Cushman, S.A., Neel, M.C., Ene, E., 2002. FRAGSTATS: Spatial Pattern Analysis Program for Categorical Maps, https://www.umass. edu/l{and}eco/research/fragstats/downloads/fragstats_downloads.html# FRAGSTATS (accessed 26/2/19). McHugh, J.L., 1967. Estuarine Nekton. In: Lauff, G.H. (Eds). Estuaries, pp. 581–620. McLusky, D.S., Elliott, M., 2007. Transitional waters: A new approach, semantics or just muddying the waters? Estuar. Coast. Shelf Sci. 71 (3–4), 359–363. http://dx.doi.org/10.1016/j.ecss.2006.08.025. McLusky, D.S., Jonge, V.N., Pomfret, J., Elliott, M., O’Reilly, M.G., Taylor, C.J.L. (Eds.), 1990. The Forth Estuary: A Nursery and Overwintering Area for North Sea Fishes: North Sea—Estuaries Interactions. Springer Netherlands, Dordrecht. Metin, G., İlkyaz, A.T., Soykan, O., Kinacigil, H.T., 2011. Age, growth and reproduction of four-spotted goby, Deltentosteus quadrimaculatus (Valenciennes, 1837), in Izmir Bay (central Aegean Sea). Turk. J. Zool. 35, 711–716. http: //dx.doi.org/10.3906/zoo-1001-32.

L. Connor, D. Ryan, R. Feeney et al. / Regional Studies in Marine Science 32 (2019) 100836 Meynecke, J.O., Lee, S.Y., Duke, N.C., 2008. Linking spatial metrics and fish catch reveals the importance of coastal wetland connectivity to inshore fisheries in Queensland, Australia. Biol. Conserv. 141 (4), 981–996, http: //www.sciencedirect.com/science/article/pii/S0006320708000463. Monaco, M.E., Lowery, T.A., R.L., Emmett, 1992. Assemblages of U.S. west coast estuaries based on the distribution of fishes. J. Biogeogr. 19 (3), 251–267, http://www.jstor.org/stable/2845450. Monteiroa, N.M., Vieira, N.M., Almada, V., 2005. Homing behaviour and individual identification of the pipefish Nerophis lumbriciformis (Pisces; Syngnathidae): a true intertidal resident? Estuar. Coast. Shelf Sci. 63, 93–99. http://dx.doi. org/10.1016/j.ecss.2004.10.012. Nakagawa, S., Johnson, P.C.D., Schielzeth, H., 2017. The coefficient of determination R2 and intra-class correlation coefficient from generalized linear mixed effects models revisited and expanded. J. R. Soc. Interface 14 (134), 20170213. Nicolas, D., Lobry, J., Lepage, M., Sautour, B., Le Pape, O., Cabral, H., et al., 2010. Fish under influence: A macroecological analysis of relations between fish species richness and environmental gradients among European tidal estuaries. Estuar. Coast. Shelf Sci. 86 (1), 137–147, http://www.sciencedirect. com/science/article/pii/S0272771409005083. NOAA, 2017. What is eutrophication? National Ocean Service - National Oceanic and Atmospheric Administration website; https://oceanservice.noaa. gov/facts/eutrophication.html.. NOAA, 2019. What is an estuary? National Ocean Service - National Oceanic and Atmospheric Administration website. Nolan, G., Gillooly, M., Whelan, K., 2010. Marine Institute. Irish Ocean Climate and Ecosystem Status Report Summary 2009. Oksanen, J., 2015. Multivariate analysis of ecological communities in R: vegan tutorial. R Doc. 1-40 http://dx.doi.org/10.1016/0169-5347(88)90124-3. Pawson, M.G., Kupschus, S., Pickett, G.D., 2007. The status of sea bass (Dicentrarchus labrax) stocks around England and Wales, derived using a separable catch-at-age model, and implications for fisheries management. ICES J. Mar. Sci. 64 (2), 346–356. http://dx.doi.org/10.1093/icesjms/fsl030. Pease, B.C., 1999. A spatially oriented analysis of estuaries and their associated commercial fisheries in New South Wales, Australia. Fish. Res. 42 (1), 67–86, http://www.sciencedirect.com/science/article/pii/S0165783699000351. Petr, T., 1999. Fish and Fisheries at Higher Altitudes: Asia. p. 180. Pickett, G.D., Brown, M., Harley, B., Dunn, M.R., 2002. Surveying fish populations in the Solent and adjacent harbours using the CEFAS bass trawl. Science Series Technical Report, CEFAS Lowestoft, 118: 16pp. Potter, I.C., Tweedley, J.R., Elliott, M., Whitfield, A.K., 2013. The ways in which fish use estuaries: A refinement and expansion of the guild approach. Fish Fish. 16 (2), 230–239. http://dx.doi.org/10.1111/faf.12050. Power, M., Attrill, M.J., Thomas, R.M., 2000. Environmental factors and interactions affecting the temporal abundance of juvenile flatfish in the Thames Estuary. J. Sea Res. 43 (2), 135–149, http://www.sciencedirect.com/science/ article/pii/S1385110100000101.

15

R Core Team, 2017. R Development Core Team, http://www.R-project.org. (accessed 26/2/19). Remane, A., 1934. Die brackwasserfauna. Verz. Veröffentlichungen Goldsteins 36, 34–74. Rijnsdorp, A.D., Peck, M.A., Engelhard, G.H., Moellmann, C., Pinnegar, J.K., 2010. Resolving climate impacts on fish stocks. Copenhagen, Denmark: ICES; ICES Research Report 301. Ryan, D., Corcoran, W., Coyne, J., O’Callaghan, R., Roche, W.K., 2016. Sampling Fish for the Water Framework Directive - Summary Report 2015: Internal Report: Inland Fisheries Ireland. Ryan, D., Corcoran, W., Coyne, J., Puttharee, D., Roche, W.K., 2017. Sampling Fish for the Water Framework Directive - Summary Report 2016: Internal Report: Inland Fisheries Ireland. Ryan, D., Corcoran, W., Coyne, J., Robson, M., Roche, W.K., 2018. Sampling Fish for the Water Framework Directive - Summary Report 2017: Internal Report: Inland Fisheries Ireland. Schallenberg, M., Hall, C.J., Burns, C.W., 2003. Consequences of climate-induced salinity increases on zooplankton abundance and diversity in coastal lakes. Mar. Ecol. Progr. Ser. 251, 181–189. http://dx.doi.org/10.3354/meps251181. Sosa-López, A., Mouillot, D., Ramos-Miranda, J., Flores-Hernandez, D., Chi, T.D., 2007. ORIGINAL ARTICLE: Fish species richness decreases with salinity in tropical coastal lagoons. J. Biogeogr. 34 (1), 52–61. http://dx.doi.org/10.1111/ j.1365-2699.2006.01588.x. Telesh, I.V., Khlebovich, V.V., 2010. Principal processes within the estuarine salinity gradient: A review. Mar. Pollut. Bull. 61 (4), 149–155, http://www. sciencedirect.com/science/article/pii/S0025326X10000755. Vasconcelos, R.P., Henriques, S., França, S., Pasquaud, S., Cardoso, I., Laborde, M., et al., 2015. Global patterns and predictors of fish species richness in estuaries. J. Anim. Ecol. 84 (5), 1331–1341. http://dx.doi.org/10.1111/13652656.12372. Went, E.J., 1978. The zoogeography of some fishes in Irish waters. Fish. Leaflet 93. Wickham, H. ggplot2, 2009. Elegant Graphics for Data Analysis. Media 35. Springer New York, New York, NY, http://dx.doi.org/10.1007/978-0-38798141-3. Wilson, J.G., Giltrap, M., Kelly, F., 2016. Fish in tidal freshwater transitional waters in ireland: Recommendations for assessment, policy and management of ecological quality under the Water Framework Directive (WFD). Biol. Environ.: Proc. R. Irish Acad. 116B (3), 221–232, http://www.jstor.org/stable/ 103318/bioe.201628. Zuur, A.F., Ieno, E.N., Elphick, C.S., 2010. A protocol for data exploration to avoid common statistical problems. Methods Ecol. Evol. 1 (1), 3–14. http: //dx.doi.org/10.1111/j.2041-210X.2009.00001.x. Zuur, A.F., Leno, E.N., Smith, G.N., 2007. Generalised linear modelling. In: Zuur, A.F., Leno, E.N., Smith, G.N. (Eds.), Analysing Ecological Data. Springer New York, New York, NY, pp. 79–96.