Estuarine, Coastal and Shelf Science 136 (2014) 112e118
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Multidecadal dynamics of larval gobies Pomatoschistus spp. in response to environmental variability in a shallow temperate bay Kerli Laur a, *, Henn Ojaveer a, Mart Simm b, Riina Klais a a b
Estonian Marine Institute, University of Tartu, Lootsi 2a, 80012 Pärnu, Estonia Estonian Marine Institute, University of Tartu, Mäealuse 14, 12618 Tallinn, Estonia
a r t i c l e i n f o
a b s t r a c t
Article history: Received 13 May 2013 Accepted 11 November 2013 Available online 18 November 2013
Compared to commercial fish, there is relatively limited information available about the dynamics of non-commercial fish that very often play important structural and functional roles in marine ecosystems. Long-term investigations that provide quantitative estimates of the population dynamics as a function of environmental variability are needed to understand the ecology and role of the non-commercial fish in the ecosystem, and assist the ecosystem management where relevant. Here we analyze the inter-annual variability and long-term trends of the abundance of the larval non-commercial gobies Pomatoschistus spp. in a shallow coastal bay (Pärnu Bay, northeastern Baltic Sea) in 1959e2010, in relation to climate and prey field related variables. The abundance of larval Pomatoschistus spp. decreased over the last 50 years along with the concomitant decrease in the water transparency. The first appearance of larvae has shifted for about two weeks earlier and is mostly related to the timing of ice cover breakdown. However, some of the effects of the environmental forcing on larval fish may be obscured by the uncertainty of species identification of individuals of the genus Pomatoschistus at larval stage, and the investigated population of Pomatoschistus spp. consists of at least two species with slightly different ecologies and also environmental preferences. Ó 2013 Elsevier Ltd. All rights reserved.
Keywords: fish larvae long-term changes abiotic factors prey density Baltic Sea coastal waters
1. Introduction In-depth knowledge of the abundance and distribution of early life-history stages provides important insights to the ecology of fish populations and communities. The most critical time in the life history of fish is the larval stage when the highest mortality occurs (Hjort, 1914; Cushing, 1975). The early life history stages of fish are particularly susceptible to the variability of the environment and are affected by both, the biological (e.g. abundance of food) as well as the physical factors such as water transparency, temperature and salinity (e.g. Fiedler, 1986; Somarakis et al., 2002; Genner et al., 2010). Temperature is an important factor controlling seasonal abundance pattern of larval fish through various mechanisms and processes (e.g. Marques et al., 2006; Genner et al., 2010). Abiotic factors, food limitation and starvation together can explain high mortality in the early larval stage, and the decline of abundance of fish larvae (e.g. Bochdansky et al., 2008), resulting either from
* Corresponding author. E-mail address:
[email protected] (K. Laur). 0272-7714/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ecss.2013.11.011
declining abundance of prey or mismatch with prey due to earlier/ later appearance. Gobies Pomatoschistus spp. are small-sized short-living abundant fish (Fonds, 1973). They constitute a significant part of demersal fish communities form the Mediterranean up to Norway including the Baltic Sea (e.g., Hesthagen, 1977; Psuty-Lipska and Garbacik-Wesolowska, 1998). In the Baltic Sea, there are at least two Pomatoschistus species: sand goby P. minutus and common goby P. microps. They are well-adapted to the brackish conditions prevailing in the estuaries (e.g. Bouchereau and Guelorget, 1998). Temperature requirements differ between the adults as P. microps is more of a warm water species (Fonds, 1973). As a consequence of lower spawning temperature, P. minutus may reproduce earlier in the season and benefit from longer period of growth before the onset of winter (Wiederholm, 1987). In northern areas gobies are known to avoid low temperatures and migrate to deeper offshore areas in winter and return to shallower areas again in March when the water temperature increases (Fonds, 1973). P. minutus is probably the first to migrate back to shallower areas to spawn and P. microps dominates in summer when the water temperature is above 20 C. Pomatoschistus spp. are batch spawners that develop and releases multiple batches of eggs within a spawning season
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(Waligóra-Borek and Sapota, 2005). Newly hatched larvae are approximately 2.5 mm long. They live pelagically for at least one month (Fonds, 1973) and change to a demersal way of life after metamorphosis (Guelinckx et al., 2008). In the Baltic Sea, Pomatoschistus spp. is shown to serve several important functions, such as being a prey for upper trophic levels (Uzars, 1994; Lundrstöm et al., 2010) and influence stock performance of commercially exploited predatory fish (Müller-Karulis et al., 2013). The current study examines the multi-decadal dynamics of the larval Pomatoschistus spp. in a shallow bay in the northeastern Baltic Sea in order to 1) describe the long-term trends in the abundance of goby larvae, 2) analyze the impact of abiotic environment and prey density on their abundance. 2. Material and methods 2.1. Study area Pärnu Bay in the northeastern Baltic Sea (Fig. 1) is a sheltered and shallow (maximum depth around 10 m) sea area covering 400 km2 with a volume of 2 km3. In most years the bay is icecovered in winters. Sea surface temperature (SST) fluctuates seasonally from regular sub-zero C with a closed ice sheet in winter to >20 C during summer. In the warm season, the water is generally well mixed down to the bottom. The currents are weak (velocity below 10 cm s1) and mainly determined by wind, but modified by coastline and bottom topography. The salinity varies from nearly freshwater at the river mouth to 7.5 psu in more open
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areas. Because of the shallowness, changes in the air temperatures directly affect the water temperature. The hydrographic conditions are formed under the complex influence of ice conditions, freshwater inputs from the Pärnu River and the water exchange with the GoR (e.g. Kotta et al., 2009). 2.2. Data, sampling procedures and laboratory analysis Sampling of fish larvae was performed weekly in six stations (Fig. 1) from May to July during daytime in 1959e2010. Locations of the stations, together with the sampling frequency, were historically placed with the intention to collect samples of ichthyoplankton representative of the study area (Pärnu Bay). These selected stations cover the study area evenly. In most cases all six stations were sampled every week (an average of 5 stations per week). Hensen larval trawl (approximately 920 mm in length) with mouth diameter of 800 mm and the mesh size 500 mm (170 mm in the cod-end sampler) was used for collecting ichthyoplankton. Sampling was performed with circular movement of the boat to keep the gear away from the disturbance caused by the boat at a speed of approx. 2 knots in the surface layer (0e1 m) by 10-min hauls. Surface sampling was adopted as the study area is very shallow with some stations characterized by depth around 3 m (Arula et al., 2012). As goby larvae are pelagic for at least one month and they adopt a demersal life style only after metamorphosis (Fonds, 1973; Guelinckx et al., 2008), it is therefore considered that the obtained data are representative to characterize dynamics of larval stages of the fish. The numbers were recalculated according
Fig. 1. Study area with six larval Pomatoschistus spp. (circles) and two zooplankton (crosses) sampling stations in Pärnu Bay (Gulf of Riga, Baltic Sea).
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to the volume of water filtered during the haul (average 275 m3 haul1, measured with flowmeter Hydro-Bios ‘Digital Flowmeter 483110’). All collected fish samples were preserved in a 4% buffered formaldehyde solution immediately after collection. Species composition of the larval samples was determined in the laboratory. Larval Pomatoschistus spp. were counted and identified in the samples at the genus level by consulting with identification keys developed by Dmitrieva (1954) (later also by Munk and Nielsen, 2005). Although identifying of larval Pomatoschistus spp. to a species level has remained as an unachievable challenge by classical taxonomy methods as yet (Munk, P., pers. comm.; Urho, L., pers. comm.), distinguishing them from other broadly similarlylooking taxa such as the larvae of perch (Perca fluviatilis) and ruffe (Gymnocephalus cernuus) has received special attention and it was ensured that no misidentification has occurred. The major key differences between goby and percid larvae lies in head shape and also the presence of swim bladder and almost lack of yolk in goby larvae at hatch (Dmitrieva, 1954; Munk and Nielsen, 2005). Prey of larval gobies e mesozooplankton e was collected from two stations (Fig. 1) which are considered representative in characterizing the dynamics of the zooplankton community composition as well as abundance and biomass in Pärnu Bay. The sampling was performed in parallel with larval fish collection by vertical hauls with a Juday net (mouth opening area 0.1 m2, mesh size 100 mm). Zooplankton sample collections and analysis for the abundance calculations (estimated from a number of subsamples) were done by a method which followed the recommendations later set out by the HELCOM (1988). Five zooplankton components were selected for the analysis (Table 1), considered as important prey items for larval Pomatoschistus spp., based on the gut content examinations in the study area (Lankov, A., unpubl. data). Water transparency was measured by Secchi depth with precision of 0.1 m throughout all larval sampling events. Ice-off day (the day of the year in which the Bay is totally free of ice cover) and air temperatures data for 1959e2010 was provided by Estonian Hydrological and Meteorological Institute. For some time series the collection methodology has changed over 50 years and therefore we had to exclude some of the valuable datasets (e.g. water temperature, salinity) used in the previous studies for shorter time scale (e.g. Parmanne and Lindström, 2003). Since the key characteristics of the study area differ from other nearby estuary sites (e.g., coastal morphology and bottom topography) thereby creating area-specific hydrological conditions, the replacing of missing factors with datasets collected elsewhere is scientifically not justified. 2.3. Statistical analysis Sampling of the larvae from 6 locations in the study area started every year before the first appearance of the larvae making it possible to detect the timing of the first appearance. The duration of Table 1 Details on the environmental variables used in the current study. No.
Description (data source)
1.
Approximate timing of the ice cover break down (Estonian Meteorological and Hydrological Institute, EMHI) Water transparency in Pärnu Bay, mean for MayeJuly, m (Estonian Marine Institute, EMI) Summer air temperature in Pärnu, monthly mean for MayeJuly, C (EMHI) Winter air temperature in Pärnu, monthly mean for JanuaryeMarch, C (EMHI) Abundance of nauplii, copepodite stages IeIII and IVeV, and adults of Eurytemora affinis, mean for MayeJuly, ind m3 (EMI) Abundance of Bosmina spp., mean for MayeJuly, ind m3 (EMI)
2. 3. 4. 5e8. 9.
sampling in weeks varied interannually (at minimum, 6 consecutive weeks were sampled, but often more). While there was no systematic difference in the abundances between different sampling stations (Fig 2A), abundances did increase markedly over the weeks 20e24 (Fig 2B). Therefore, to compute comparable yearly means of larval goby abundance, unbiased by the sampling duration of any particular year, a linear model with two categorical factors (year and week) was fitted to the data:
Yij ¼ weeki þ yearj þ eij
(1)
where Yij is the expectation for the log-transformed mean abundance at week i and year j, eij is a normal distributed random error, weeki is the mean abundance for each level of factor week and yearj is the mean abundance for each level of factor year. Comparable yearly means were calculated by computing the marginal distribution for each level of factor year from the linear combination of the parameter estimates in Eq (1), confidence intervals reported are the 1.96 standard errors of the parameter estimates. Same method was used for calculating the yearly means of the zooplankton variables, except that in the zooplankton model, also the sampling station was included as a categorical explanatory variable with two levels. Linear regression was fitted through the yearly means of goby larvae (year as a continuous predictor) to estimate the magnitude of the long-term change in the abundance. A non-parametric ManneKendall trend test was used to detect the presence of long-term trends all other variables, the yearly estimates of zooplankton abundance, water transparency and winter and summer air temperatures (Table 1). The non-parametric Manne Kendall test was chosen because of the non-linear appearance of most of the trends. The Spearman rank correlation was used to quantify the association between the first appearance of goby larvae and ice-off day and winter air temperatures. The generalized additive model (GAM, Wood, 2006) smoother was used to visualize the relationship between ice-off day and first appearance of goby larvae. The environmental effects on the yearly mean abundance of larvae were first assessed by multivariate linear regression with the yearly means of water transparency, winter and summer air temperatures and zooplankton abundance (Eurytemora affinis nauplii, copepodites and adult copepods, and cladoceran Bosmina spp.) as explanatory variables. The significant effects were identified by the backward elimination, where the least important factors were removed one at the time, followed by refitting the model and comparing the previous and new model AIC values at each step. Yearly means of goby larvae show significant temporal autocorrelation at lag 1 that disappeared after the long-term trend was removed. A significant long-term trend was also present in winter air temperatures and water transparency time series, and significant positive autocorrelation remained in the water transparency time-series also after detrending. However, as the positive autocorrelation in the dependent variable, the goby larvae, was only due to the long-term trend, we did not consider it essential to be accounted for in the models. Instead, to identify whether the cause of the significant correlation (or the absence of correlation) is the presence of the concomitant trends in the variables, we separated the variables with a significant long-term time trends into the trend and residual components, and analyzed the associations between the residuals. This approach has been recently proven to be useful in studies with Iberian sardine recruitment in relation to environment (Santos et al., 2012). Statistical analyses were performed in R (R Development Core Team, 2012), GAM models were constructed using the gam function form the library mgcv (Wood, 2006).
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Fig. 2. Box and whisker plots of log-transformed abundance of goby larvae between the six sampling locations (A) and between the sampling weeks (B).
From all four abiotic long-term time-series, the winter air temperatures (MannKendall’s tau ¼ 0.26, p ¼ 0.02) showed a significant positive whereas water transparency (MannKendall’s tau ¼ 0.43, p < 0.001) showed a significant negative timetrend (Fig 3). Copepod nauplii show a significant long-term decreasing trend, with substantial decadal-scale variability in abundance (Fig 4A). Long-term trends in other five investigated zooplankton taxa were not significant (Fig 4).
The timing of the first appearance of larvae varies over a month (Year-days 133 to 176, Fig 6A). On average, goby larvae first appear in late May or in the beginning of June in samples taken from the northern part of Pärnu Bay. There was a statistically significant seasonal advancement in the timing of the first appearance of larvae, approximately 12 days (based on the slope parameter 0.22 days per year, over 52 years; p ¼ 0.02) (Fig 6A). The timing of the first appearance appears to be related to the approximate timing of the ice cover break down (Spearman’s rho ¼ 0.53; Fig 6B) e larvae never appeared earlier than 3 weeks after the ice cover break down, but also not before the beginning of May (day 133). Higher residual variation was observed for early ice break down.
3.2. Long-term trends in the abundance and first appearance of goby larvae
3.3. Impact of abiotic environment and prey density on the abundance of goby larvae
Seasonally the abundance of goby larvae can vary from only a few up to >2000 individuals per 103 m3. The lowest values were recorded in the early 1980s and mid-2000s, and the highest at the beginning of the study period (year 1959). The mean abundance of goby larvae has decreased nearly fourfold over the 50 years observation period, judging from the linear trend in the yearly mean abundances (slope ¼ 0.02, p ¼ 0.005, n ¼ 43, Fig 5), from about 41 specimens to about 11 specimens per 103 m3. The decreasing trend appears consistent in time and does not arise from a few high values at the beginning of the observation period. Also, yearly means were estimated on average from 43 samples (min 25, max 69), and according to the Cyr et al., 1992, 40 samples (per year) is sufficient to detect fourfold difference between two means at average density of 30 larvae per sample at significance level of 0.05.
In a statistical modeling of the yearly mean abundance of goby larvae as a function of a set of abiotic variables and zooplankton, all except the water transparency were excluded by backward elimination from the model where the yearly mean of goby abundance was the response variable. Water transparency had a positive effect on goby larvae (slope ¼ 0.72, R2 ¼ 0.07, p ¼ 0.05), meaning that if transparency increases by 1.6 m (the difference between minimum and maximum value of the water transparency during 1959e2010), the average abundance of goby larvae increases approximately 3.2 times. However, the model with residual variation of water transparency and winter air temperatures revealed no significant effects on the larval goby abundance, implying that the significant effect of water transparency arises from the concomitant long-term trends between the goby larvae and water transparency.
3. Results 3.1. Long-term trends of the biotic and abiotic environment
Fig. 3. Time series of abiotic parameters with Mann Kendall test for: A) monthly average air temperature sum in winter (JanuaryeMarch, C) in Pärnu (gray line with linear trend); monthly average air temperature in summer (MayeJuly, C) in Pärnu (black line); B) water transparency (m) in Pärnu Bay (black line with linear trend). For details and data origin, please see Table 1.
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Fig. 4. Long-term dynamics (log-transformed abundance ind m3) of (A) Eurytemora affinis nauplii (B) E. affinis copepodite stages I‒III; (C) E. affinis copepodite stages IV‒V; (D) E. affinis adults; (E) Bosmina spp. in Pärnu Bay (Gulf of Riga, Baltic Sea) in 1959e2010.
Separating the years into cold and warm ones did not improve the predictive power of environmental variables but, in cold years, water transparency still showed the marginally significant positive effect on goby larvae annual abundance (p ¼ 0.06). 4. Discussion
Fig. 5. Yearly means and long-term linear trend in the larval goby abundance. Larger filled circles denote the yearly means, calculated with generalized linear model, equipped with the confidence intervals of parameter standard errors. Smaller filled circles denote the single observations, colored with alpha channel for better visualization of the density of overlaying points. Trend line and slope value are from the linear model of the yearly means versus the year of observation, and the fitted values decline from 41 individuals to 11 individuals per 100 m3 when back-transformed from logarithmic scale.
We have found a notable interannual variability in the average abundance of goby larvae (approximately four-fold) with a general long-term declining trend. This trend was accompanied by the decrease in water transparency. As Pomatoschistus spp. are batch spawners, their larval abundance probably represents a combination of the population size and the reproductive effort of the available population. We also note a seasonal advancement of the first appearance of larvae in the plankton. The Pomatoschistus spp. taxon in the study area probably consists of at least two species: P. minutus and P. microps. These species have slightly different ecological requirements with respect to salinity and temperature variations (Fonds and van Buurt, 1974). Although these two species can occupy different areas (Leitão et al., 2006; Dolbeth et al., 2007), they often co-occur and compete for food and (Pampoulie et al., 2000) and nesting habitat (Lindström and Pampoulie, 2005). A three-fold variation in the abundance of larval Pomatoschistus spp. has been reported in earlier studies from the Baltic Sea, e.g., during 1970s to 1990s. In Bothnian Bay and Western Gulf of Finland the average number of larvae during 1974e1996 was 0.27 0.69
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Fig. 6. (A) The first appearance of larval Pomatoschistus spp. in Pärnu Bay (Gulf of Riga, Baltic Sea) with Mann Kendall’s trend line; (B) relationship between first appearance of larval Pomatoschistus spp. and ice cover day-off in Pärnu Bay during 1959e2010. Solid line represents GAM-fitted line drawn for the data and dotted line indicates the double standard error.
individuals per m3 (mean S.D.) (Parmanne and Lindström, 2003). Although yearly mean abundances in Pärnu Bay were higher in 1960s, they have now decreased below the abundances reported for the Bothnia Bay. Such notable shifts in the abundance of species call for attention, as the local food-web structure can change greatly in response to fluctuations in the abundance of any community member (Mittelbach et al., 1988; Elser et al., 1995). Distribution and abundance of fish larvae depends on multiple factors that include the abiotic environment (Somarakis et al., 2002). In our data, the long-term decline of larval abundance was accompanied by a long-term decrease in the water transparency, although the residual variation around the long term trend was not correlated to the detrended water transparency. Declining water transparency could therefore lower the baseline for larval abundance, but there must be other factors determining the observed inter-annual variability. Water transparency in Pärnu Bay is shaped by winds, primary production and shipping activity. Winds and shipping cause intensive resuspension of sediments, potentially
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overshadowing other factors such as phytoplankton and the concentration of chlorophyll a (Wasmund et al., 2001; Paavel et al., 2011). There are several ways that the low water transparency can be detrimental for the larvae. Fish larvae feeding on zooplankton depend on vision in their search for prey (Guthrie, 1986) and therefore increased turbidity of the water can reduce larval feeding and reaction distance as well as the contrast between the prey and its background (Pekcan-Hekin, 2007). Larvae are prone to abrasion damage and other potentially sublethal effects, when in contact with resuspended sediments (Boehlert, 1984) as epidermis of early larvae of many fish species is only a few cells thick (O’Connell, 1981). This can also be fatal to goby larvae as they are slender and very small at hatching (2.4e2.6 mm) (Borges et al., 2011). High turbidity can decrease mate choice and weaken sexual selection (Järvenpää and Lindström, 2004; Candolin et al., 2007) and thereby also potentially reduce the reproduction success, incl. larval abundance. Water transparency can also influence the predation pressure. One of the most important predators for goby larvae in the study area is young pikeperch. They start feeding on goby larvae at the length of 3 cm. As pikeperch are known to have “spying” feeding behavior, the predation is more effective at lower transparencies (Erm, 1981). Thermal regime modifies density dynamics of fish larvae through various ways (e.g. Genner et al., 2010). Amongst others, it has been shown that winter severity has significant influence on annual abundance dynamics of Pomatoschistus spp. larvae (Parmanne and Lindström, 2003). The temperature effect may be masked by the presence of more than one species with different preferences for the ambient temperature, but also due to specifics of the particular environment, i.e. no stratification during the main reproductive season resulting in complete vertical mixing down to the bottom and thereby securing favorable thermal conditions. The studied area is also an important nursery ground for larval herring (Höök et al., 2008), and recent work from the same area proposed that small herring larvae may be food limited (Arula et al., 2012). Pomatoschistus spp. larvae consume broadly a similar prey as herring larvae, although the exact diet of goby larvae is relatively poorly known. As a very simple and robust test, we incorporated the yearly mean abundances of potential prey items (copepod nauplii and copepodites) as explanatory variables in the linear regression, but found no obvious relation between goby larvae and their prey abundances. However, this type of correlation, or lack of correlation, does allow us to reach conclusions regarding the potential food limitation of larvae. More detailed investigations, starting with the gut content analyses and determination of the diet composition will be required to properly identify the role of prey in larval goby growth, survival and abundance dynamics. The timing of the first appearance of larvae can also result from the changing proportions of two species. A visual inspection of the individual years indicated that the overall seasonal dynamics, for example the timing of maximum abundance, did not change with the timing of the first appearance. The variation in the first appearance, especially when the ice break off was early in the season, was probably caused by sporadic spawning of a small number of individuals, likely the species adapted to lower temperatures. A major drawback of the current work is that the analyzed abundances consist of at least two species with slightly different environmental preferences/tolerances and migratory behavior. Therefore, annual abundance estimates, as well as the first appearance of larvae may be influenced by changes in species relative abundances, the extent of which remains unclear as the identification of goby larvae to a species level is proved to be
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unreliable by classical morphological taxonomy. In addition, there were also some gaps in the data. The uneven sampling, particularly in the beginning of the season, was corrected by using the linear regression model for calculating the balanced means. The missing years (11 years out of the 52 year period) in the data, mostly due to the lack of resources to carry out comparable sampling effort, were not accounted for in the analyses and we do not consider that they would have changed the results in a systematic way. There was no tendency for more missing years in the beginning or end of the time series, hence the trend was not affected. Also, there was no temporal autocorrelation between the sequential years, apart from that caused by the long-term trend. Hence, we do not consider that missing some years would have biased the results in any other way than just reducing slightly the power of the tests due to reduced number of observations.
Acknowledgments This work was partially financed by the Estonian Ministry of Education and Research (grant SF0180005s10), by institutional research funding IUT02-20 of the Estonian Research Council and the Estonian Science Foundation (grant 8747). The research leading to these results has also received funding from the European Community’s Seventh Framework Programme (FP7/2007e2013) under Grant Agreement No. 266445 for the Vectors Change in Oceans and Seas marine Life, Impact on Economics Sectors (VECTORS). The study has been partly supported by the project “The status of marine biodiversity and its potential futures in the Estonian coastal sea” 3.2.0802.11-0029 of Environmental protection and technology programme of European Regional Fund. We also thank two anonymous reviewers whose comments significantly helped to improve the manuscript.
References Arula, T., Kotta, J., Lankov, A., Simm, M., Põlme, S., 2012. Diet composition and feeding activity of larval spring-spawning herring: importance of environmental variability. J. Sea Res. 68, 33e40. Bochdansky, A.B., Grønkjær, P., Pepin, P., Leggett, W.C., 2008. Food limitation in fish: ontogenetic variation in feeding scope and its potential effect on survival. Mar. Ecol. Prog. Ser. 367, 239e248. Boehlert, G.W., 1984. Abrasive effects of Mount Saint Helens ash upon epidermis of yolk sac larvae of Pacific herring Clupea harengus pallasi. Mar. Environ. Res. 12, 113e126. Borges, R., Faria, C., Gil, F., Gonçalves, E.J., 2011. Early development of gobies. In: Patzner, R., Van Tassell, J.L., Kovacic, M., Kapoor, B.G. (Eds.), The Biology of Gobies. Science Publishers, USA, pp. 403e464. Bouchereau, J.L., Guelorget, O., 1998. Comparison of three Gobiidae (Teleostei) life history strategies over their geographical range. Oceanol. Acta 21, 503e517. Candolin, U., Salesto, T., Evers, M., 2007. Changed environmental conditions weaken sexual selection in sticklebacks. J. Evol. Biol. 20, 233e239. Cushing, D.H., 1975. Marine Ecology and Fisheries. Cambridge University Press, Cambridge, New York, p. 278. Cyr, H., Downing, J.A., Lalonde, S., Baines, S.B., Pace, M.L., 1992. Sampling larval fish populations: choice of sample number and size. Trans. Am. Fish. Soc. 121, 356e368. Dmitrieva, N.A., 1954. Biology and Fisheries of the Main Commercial Fish of the Baltic Sea, Tom 26. Russian Federal Research Institute of Fisheries and Oceanography (VNIRO), Trudõ, pp. 253e256 (in Russian). Dolbeth, M., Martinho, F., Leitão, R., Cabral, H., Pardal, M.A., 2007. Strategies of Pomatoschistus minutus and Pomatoschistus microps to cope with environmental instability. Estuar. Coast. Shelf Sci. 74, 263e273. Elser, J.J., Lubnow, F.S., Marzolf, E.R., Brett, M.T., Dion, G., Goldman, C.R., 1995. Factors associated with interannual and intraannual variation in nutrient limitation of phytoplankton growth in Castle Lake, California. Can. J. Fish. Aquat. Sci. 52, 93e104. Erm, V., 1981. Pikeperch (in Estonian). Valgus, Tallinn, Estonia, p. 128. Fiedler, P.C., 1986. Offshore entrainment of anchovy spawning habitat, eggs, and larvae by a displaced eddy in 1985. Calif. Coop. Ocean. Fish. Investig. Rep. 17, 144e152. Fonds, M., 1973. Sand gobies in the Dutch Wadden sea (Pomatoschistus, Gobiidae, Pisces). Neth. J. Sea Res. 6, 417e478.
Fonds, M., van Buurt, G., 1974. The influence of temperature and salinity on the development and survival of goby eggs (Pisces, Gobiidae). Hydrobiol. Bull. 8, 110e116. Genner, M.J., Halliday, N.C., Simpson, S.D., Southward, A.J., Hawkins, S.J., Sims, D.W., 2010. Temperature-driven phenological changes within a marine larval fish assemblage. J. Plankton Res. 32, 699e708. Guelinckx, J., Maes, J., Geysen, B., Ollevier, F., 2008. Estuarine recruitment of a marine goby reconstructed with an isotopic clock. Oecologia 157, 41e52. Guthrie, D.M., 1986. Role of vision in fish behaviour. In: Pitcher, T.J. (Ed.), The Behaviour of Teleost Fishes. Croom Helm, London, pp. 75e113. HELCOM, 1988. Guidelines for the Baltic monitoring programme for the third stage. In: Baltic Sea Environmental Proceedings No 27D. HELCOM, Helsinki. Hesthagen, I.H., 1977. Migrations, breeding and growth in Pomatoschistus minutus (Pallas) (Pisces, Gobiidae) in Oslofjorden, Norway. Sarsia 63, 17e26. Hjort, J., 1914. Fluctuations in the Great Fisheries of Northern Europe. Rapports et Procès e verbaux des Réunions. Cons. Perm. Int. Expl. Mer 20, 1e228. Höök, T.O., Gorokhova, E., Hansson, S., 2008. RNA: DNA ratios of Baltic Sea herring larvae and copepods in embayment and open sea habitats. Estuar. Coast. Shelf Sci. 76, 29e35. Järvenpää, M., Lindström, K., 2004. Water turbidity by algal blooms causes mating system breakdown in a shallow-water fish, the sand goby Pomatoschistus minutus. Proc. R. Soc. B-Biolog. Sci. 271, 2361e2365. Kotta, J., Kotta, I., Simm, M., Põllupüü, M., 2009. Separate and interactive effects of eutrophication and climate variables on the ecosystem elements of the Gulf of Riga. Estuar. Coast. Shelf Sci. 84, 509e518. Leitão, R., Martinho, F., Neto, J.M., Cabral, H., Marques, J.C., Pardal, M.A., 2006. Feeding ecology, population structure and distribution of Pomatoschistus microps (Krøyer, 1838) and Pomatoschistus minutus (Pallas, 1770) in a temperate estuary, Portugal. Estuar. Coast. Shelf Sci. 66, 231e239. Lindström, K., Pampoulie, C., 2005. Effects of resource holding potential and resource value on tenure at nest sites in sand gobies. Behav. Ecol. 16, 70e74. Lundrstöm, K., Hjerne, O., Lunneryd, S.-G., Karlsson, O., 2010. Understanding the diet composition of marine mammals: grey seals (Halichoerus grypus) in the Baltic Sea. ICES J. Mar. Sci. 67, 1230e1239. Marques, S.C., Azeiteiro, U.M., Marques, J.C., Neto, J.M., Pardal, M.A., 2006. Zooplankton and ichthyoplankton communities in a temperate estuary: spatial and temporal patterns. J. Plankton Res. 28, 297e312. Mittelbach, G.G., Osenberg, C.W., Leibold, M.A., 1988. Trophic relations and ontogenetic niche shifts in aquatic ecosystems. In: Ebenman, B., Persson, L. (Eds.), Size-structured Populations: Ecology and Evolution. Springer-Verlag, Berlin, pp. 219e235. Müller-Karulis, B., Arula, T., Balode, M., Laur, K., Ojaveer, E., 2013. Challenges and opportunities of local fisheries management: pikeperch, Sander lucioperca (Actinopterygii: Perciformes: Percidae), in Pärnu Bay, northern Gulf of Riga, Baltic Sea. Acta Ichthyol. Pisca. 43, 151e161. Munk, P., Nielsen, J.G., 2005. Eggs and Larvae of North Sea Fishes. Biofolia, Denmark, p. 215. O’Connell, C.P., 1981. Development of organ systems in the northern anchovy, Engraulis mordax and other teleosts. Am. Zool. 21, 429e446. Paavel, B., Arst, H., Metsamaa, L., Toming, K., Reinart, A., 2011. Optical investigations of CDOM-rich coastal waters in Pärnu Bay. Eston. J. Earth Sci. 60, 102e112. Pampoulie, C., Bouchereau, J.L., Rosecchi, E., Poizat, G., Crivelli, A.J., 2000. Annual variations in the reproductive traits of Pomatoschistus microps in a Mediterranean lagoon undergoing environmental changes: evidence of phenotypic plasticity. J. Fish. Biol. 57, 1441e1452. Parmanne, R., Lindström, K., 2003. Annual variation in gobiid larval density in the northern Baltic Sea. J. Fish. Biol. 62, 413e426. Pekcan-Hekin, Z., 2007. Effects of Turbidity on Feeding and Distribution of Fish. Academic dissertation. University of Helsinki, Finland, p. 39. Psuty-Lipska, I., Garbacik-Weso1owska, A., 1998. Species composition and fish distribution in the Pomeranian Bay and Szczecin Lagoon. Bull. Sea Fish. Inst. 3, 3e20. R Development Core Team, 2012. R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Santos, M.B., González-Quirós, R., Riveiro, I., Cabanas, J.M., Porteiro, C., Pierce, G.J., 2012. Cycles, trends, and residual variation in the Iberian sardine (Sardina pilchardus) recruitment series and their relationship with the environment. Ices J. Mar. Sci. 69, 739e750. Somarakis, S., Drakopoulos, P., Filippou, V., 2002. Distribution and abundance of larval fish in the northern Aegean Sea - eastern Mediterranean e in relation to early summer oceanographic conditions. J. Plankton Res. 24, 339e358. Uzars, D., 1994. Feeding of cod (Gadus morhua callarias L.) in the central Baltic in relation to environmental changes. ICES Mar. Sci. Symp. 198, 612e623. Waligóra-Borek, K., Sapota, M.R., 2005. Breeding characteristics of the sand goby (Pomatoschistus minutus) e one of the most abundant goby species in the coastal waters of the Gulf of Gdansk region (Southern Baltic Sea). Oceanol. Hydrobiol. Stud. 34, 47e55. Wasmund, N., Voss, M., Lochte, K., 2001. Evidence of nitrogen fixation by nonheterocystous cyanobacteria in the Baltic Sea and recalculation of a budget of nitrogen fixation. Mar. Ecol. Prog. Ser. 214, 1e14. Wiederholm, A., 1987. Distribution of Pomatoschistus Minutus and Pomatoschistus microps in the Bothnian Sea: importance of salinity and temperature. Memo. Soc. Fauna Flora Fenn. 63, 56e62. Wood, S.N., 2006. Generalized Additive Models. An introduction with R. Chapman & Hall. CRC.
