ICES CM 2007/R:04

Not to be cited without prior reference to the author

Linking large- and small-scale fish surveys with the feeding ecology of seabirds

Andreas Dänhardt & Peter H. Becker

ABSTRACT The state of fish populations and stocks is annually assessed by means of extensive survey programmes as the basis for fisheries management. Yet since standard research vessels are restricted to deeper water, shallow coastal areas of the North Sea ecosystem pivotal to particular stages in the life cycles of target and non-target species are not covered. Local surveys are often limited in space and/ or time and are not coupled to the regular North Sea wide surveys. The is a large intertidal zone, serving many ecologically and economically important fish species as a nursery, including herring, sprat, plaice, sole, cod and whiting, which together account for more than 75 % in weight of annual catches North Sea wide. In addition to their meaning to recruitment processes to the adult stock (and eventually to the fishery), the juvenile stages of these species also provide the nutritional basis for piscivorous seabirds that breed in large numbers along the North Sea coasts and have synchronized their reproductive phenology with the availability of their prey fish. Based on seasonal, diurnal and tidal cycles of fish occurrence we describe principles for monitoring fish in the Wadden Sea considering relevant phenological aspects. We suggest a link with offshore sampling programmes and propose an integration of the large- and small-scale survey programmes to be put into context with seabird feeding ecology.

Contact author: Andreas Dänhardt, Institute of Avian Research, c/o Research Center Terramare, Schleusenstraße 1, 26382 , . Tel: +49 42 21 94 42 05, cell: +49 1 79 5 17 15 36, fax: +49 44 21 94 42 99, e-mail: [email protected]

INTRODUCTION

To define how and where human activities affect ecosystems is subject to a high level of uncertainty. Consequently, precautionary approaches in terms of human activities are required, and the levels of precaution should be proportional to the amount of information available such that the less is known about a system, the more precautionary management decisions should be (Marasco et al. 2007). These approaches may be perceived as overprotection unnecessarily restricting the utilization of natural goods and services while reducing the credibility of scientific advice (Langton et al. 1996), and are thus often not applied. Uncertainty can be reduced by identifying and quantifying functional relationships and food web interactions with special emphasis on spatio-temporal variation of biological (migrations, predator-prey overlap) and physical (variability of climatic- oceanic conditions at different scales) parameters. The North Sea is among the most heavily fished seas world-wide, and every year the state of fish populations and stocks is assessed by means of extensive survey programmes as the basis for managing fisheries (Flöter & Temming 2003). Yet components of the North Sea ecosystem pivotal to particular stages in the life cycles of target as well as non-target species -especially shallow coastal areas- are not covered, since large standard research vessels are restricted to deeper water. Local surveys are limited in space and/ or time (Vorberg et al. 2005) and are not coupled to the regular North Sea wide surveys. Moreover, they do not equally represent pelagic and benthic elements of the fish fauna. The Wadden Sea is Europe’s largest marine wetland and provides essential habitat for the early life stages of many ecologically and economically important fish species (Zijlstra 1978, Lozan et al. 2003), such as herring Clupea harengus, sprat Sprattus sprattus, plaice Pleuronectes platessa, sole Solea solea, cod Gadus morhua and whiting Merlangius merlangus, which together account for more than 75 % of annual catches North Sea wide (2003: 1 253 500 t, 176 500 t, 141 300 t, 17 900 t, 78 000 t and 43 200 t, respectively, Gröhsler and Zimmermann 2003). Due to its great productivity and area (22 000 km², Marencic and Essink 2005) the Wadden Sea not only provides an important nursery for the early life stages of many fish species, but also feeding and breeding habitat for a large number of migratory and breeding birds (Koffijberg et al. 2005, Blew et al. 2005), many of which utilise small fish as their main food source. Regular counts of breeding and migratory birds are carried out as part of the Trilateral Monitoring and Assessment Program (TMAG 1997), but this unique inventory does not account for the causes of the variability observed. In addition to time series of animals’ abundance, which are only able to show the effects of circumstances already affecting the monitored organisms, the detection and interpretation of (and possible reactions to) change requires the regular and long-term investigation of specific life history parameters and their responsiveness to changes e. g. food availability (Thyen et al. 1998, Becker 2003). For long-lived animals, such as most seabirds, life history theory predicts a reduction of their investment in current reproduction in years of poor food supplies, increased predation or bad weather in order to increase residual reproductive value and maximise lifetime reproductive success (Stearns 1992), so the surveillance of selected seabird colonies that are representative for populations may serve as an early warning system (Thyen et al. 1998, Furness et al. 2003). A number of traits in the life history of seabirds have been assigned suitability for monitoring environmental change (Tasker & Furness 2003), including breeding success (Croxall and Rothery 1991), variation in egg laying date (Becker 1996), egg size (Pons 1992), clutch size (Monaghan et al. 1992, Becker 1998), chick provisioning rates (Uttley 1992, Uttley et al. 1994), chick growth rates (Greenstreet et al. 1999), intensity of kleptoparasitism (Ludwigs 1998), adult and fledgling body mass (Becker et al. 2001a) and survival rates of adults and subadults (Furness et al. 2003). The extent to which food abundance is reflected by reproductive success is not uniform among seabird species, ranging from relative indifference (e. g. Northern Fulmar Fulmarus glacialis , Common Guillemot Uria aalge ) to high sensitivity (e. g. Common Sterna hirundo ) to environmental variation. Based on seasonal, diurnal and tidal cycles of fish occurrence we describe principles for monitoring fish in the Wadden Sea considering relevant phenological aspects. We suggest a possible link with offshore sampling programmes and propose an integration of the large- and small-scale survey programmes to be put into context with seabird feeding ecology.

MATERIAL & METHODS

Data on fish species composition and length class distribution (not considered in this paper) were obtained from two sources: 1. A stow net was operated at least twice per month (depending on wind conditions) with an anchoring stow net cutter in the central Jade Bay (53°28 N, 08°12 E, 4 in Fig. 1) and south-east of the Wadden Sea island Minsener Oog (53°44 N, 08°02 E, 3 in Fig. 1) between April 20 th and September 5 th 2006. The mouth opening was 5 x 7 m, the mesh size (between knots) decreased from 20 mm close to the mouth to 5 mm in the codend. Due the small size of the meshes, the resistance of the filtering net surface against the water current caused the lower beam to be lifted, so that the vertical net opening changed as a function of the current velocity, varying between 4 and 5 m. Absolute catch numbers were thus normalized to individuals per 10 000 m 3 filterend water volume. Catches were obtained from the water surface down to 4-5 m at absolute water depths of 5-8 m, depending on the tidal hour, so that pelagic fish is thought to be represented well, demersal fish however may not have been quantitavely sampled. 2. Fish retained by trash screens at the cooling water intake of a power plant at the Jade, Northern Germany (53°33 N, 08°09 E, 5 in Fig. 1) were sampled between January 3 rd and December 19 th 2006. The cooling water was extracted directly from the Jade water body at a depth of 9 m below average low water level. The water volume taken by the power plants’ turbine was quite variable and due to comparability reasons with the stow net catches and literature data, fish collected from the cooling water were also expressed as n 10 000 m -3. As the basis for the seasonal variability of the Wadden Sea fish fauna, sampling at the cooling water intake was carried out fortnightly between January and March and September and December, and twice per week between April and August. On four occasions (August 1 st and 2 nd 2005, October 25 th and 26 th 2005, July 19 th and 20 th 2006 and October 24 th and 25 th 2006) 24 h-samplings were conducted (one haul every 2 hours = 12 hauls within 24 hours) to investigate tidal and diurnal variation in fish abundance. Common (Sterna hirundo ) and Arctic ( Sterna paradisaea ) were used as representative examples of fish eating seabirds. The breeding biology in two of the largest tern colonies along the Lower Saxon Wadden Sea coast (Minsener Oog, 53°45 N, 08°.01 E, at the outer Jade and Banter See, 53°30 N, 08°05 E, in Wilhelmshaven, 1 and 2 in Fig. 1, respectively) was investigated. Parameters on breeding phenology such as first arrivals, arrival peak, first eggs, egg peak, first chicks hatched, hatching peak, first fledglings, fledging peak and breakup of the colonies were noted at the colony in Wilhelmshaven for Common Terns. At the colony site on Minsener Oog prey fed to chicks was identified to lowest possible taxonomic level and the size of prey organisms relative to the average beak length (Glutz v. Blotzheim & Bauer 1999) was determined, using binoculars (magnification 10 x 42). Feeding observations were conducted throughout July 2006 and were synchronized with the stow net fishery. A literature search was carried out to compile information on local, regional and international fish survey programmes. In addition, persons in charge of the organsation and implementation of the surveys were interviewed for recent changes and developments with the programmes.

1 3

5 2 4

Figure 1: Area investigated. Breeding colony (1) on Minsener Oog and (2) in Wilhelmshaven, (3) catch position of the stow net fishery near Minsener Oog and (4) in the central Jade Bay, (5) power plant extracting cooling water from the inner Jade.

RESULTS

Seasonal variation

Individual numbers per 10 000 m³ filtered water volume of the six species investigated in this paper varied substantially over the course of the season (Fig. 2). There was a marked variability of catch numbers between the different stages of the tidal cycle (ebb, flood, high and low water), but the general trend of increase or decrease over the season remained clear despite tidal effects. Since samples were mainly taken during the day, daytime effects were not considered with the investigation of the seasonal phenomena (Fig. 2). Herring numbers started to increase in the middle of May. Around July 20th, all herring dissappeared from the area. The presence of large numbers of herring was detected in both cooling water and stow net catches, but the quantity of fish obtained from both methods differed considerably: While cooling water catches revealed a maximum density of 80 herring per 10 000 m³ fished water volume, 750 and 25 000 individuals per 10 000 m³ were caught by the stow net in the central Jade Bay and near Minsener Oog, respectively (Figs. 2 and 3). Sprat numbers peaked six weeks later than those of herring, in August and September. A smaller peak between the end of March and the middle of May could be detected in the cooling water catches only. Sprat numbers remained relatively high until the end of October, which became evident only in the cooling water catches, since stow net catches were discontinued in the beginning of September. Maximum sprat catches collected with the stow net were two (Jade Bay) to three (Minsener Oog) orders of magnitude higher than those obtained from the cooling water intake (Figs. 2 and 3). Plaice were caught in highest numbers between mid June and the end of August, a trend that was noticed in both stow net and cooling water samples. Stow net catch numbers for plaice were again higher than those from the cooling water intake, yet the difference was less pronounced than with the clupeids (Figs. 2 and 3).. The first abundance peak of sole occurred in the middle of April, two weeks prior to the commencement of the stow net fishery. At Minsener Oog, this species was caught only on three occasions, while sole regularly appeared in both the stow net catches in the Jade Bay and in the cooling water at the inner Jade. From these two locations, an abundance peak became evident in June and July. Three to four weeks later, relatively high numbers of sole were caught near Minsener Oog with the stow net. Maximum numbers of sole per 10 000 m³ were 7, 450 and 20 individuals collected by the cooling water intake, the stow net in the Jade Bay and at Minsener Oog, respectively (Figs. 2 and 3).. In the beginning of June high numbers (230 ind. 10 000m -3) of cod were caught by the stow net in central Jade Bay. This singular event could be followed neither in the cooling water nor in the stow net catches at Minsener Oog, where cod occurred in the catches only on three occasions in the middle of May, the end of July and in the beginning of September, in relatively stable numbers. A seasonality with peaking numbers in late May only became evident in the cooling water catches (Figs. 2 and 3). As with cod, high numbers (190 ind. 10 000m -3) of whiting in the Jade Bay were only caught in the beginning of June. Until April, no whiting were caught in the cooling water. In general, whiting were caught mainly in May and June. Apart from the sporadically high catch numbers mentioned above, whiting and cod were the least numerous of the six fish species investigated. Contrary to the assumption that the cooling water intake would better represent demersal fish and the stow net catches were more appropriate to catch pelagic species (for specifications of the catch methods see material and method section), stow net catches were generally larger than those obtained from the cooling water intake. Despite the stow net catch stations in the central Jade Bay and near Minsener Oog being less than 30 km apart, differences in catch numbers are substantial, especially in clupeids, where maximum catch numbers at Minsener Oog exceeded those from the Jade Bay by a factor of 10. The frequency and the magnitude of sole catches were higher in the Jade Bay, presumably due to spawning events occurring in this area.

120 Herring Ebb tide Whiting 100 Flood tide High water 80 Low water 60 40 20 0 13 Sprat Cod 11

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Figure 2: Seasonal catches of herring, sprat, cod, whiting, plaice and sole obtained from the cooling water intake from the power plant in Wilhelmshaven. 3000 Ebb tide Jade Bay 2500 Flood tide 2000

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Figure 3: Seasonal catches of herring, sprat, cod, whiting, plaice and sole obtained from stow net catches in the central Jade Bay and near Minsener Oog. Samples were collected between April 20 th and September 5 th 2006.

Tidal and diurnal variation

Across species, abundance maxima were primarily related to ebb tide and low water (Fig. 4). The exception among the six species investigated was herring, where abundance maxima were observed around high and low water alike, so that no clear connection to the tide or the daytime could be established. Even though sprat is a pelagic species, too, its abundance patterns were more similar to those of the demersal species cod, whiting, plaice and sole, where in the majority of cases abundance maxima became evident in ebb and low water catches (Fig. 4). Lowest catch numbers were associated with flood and high water during the day in all species except herring (see above). Except for 24 th & 25 th of October 2006, herring numbers peaked at night, independent of the tidal hour. Despite sprat displaying a similar lifestyle to herring, high catch numbers were associated with low water rather than to any particular daytime. Plaice numbers increased before low water, more so at night than during the day. In sole, peak abundance around low water was evident, without a clear difference between night and daylight hours. In cod and whiting, no clear association with the daytime could be detected, probably due to the small sample size.

01. & 02.08.2005 25. & 26.10.2005 19. & 20.07.2006 24. & 25.10.2006

HW: 10:39, 23:24, 11:50 HW: 06:04, 18:46, 07:02 HW: 07:53, 20:18, 08:50 HW: 14:53, 03:05 LW: 16:57, 05:30 LW: 11:23, 00:41 LW: 13:54, 02:34 LW: 08:58, 21:10, 09:25 6 50 1,0 1,5 5 Herring 40 Herring Herring 0,8 4 1,2 30 0,6 Herring 3 0,9 20 0,4 2 0,6 1 10 0,3 0,2 0 0 0,0 0,0 30 1,0 4 1,5 25 Sprat 0,8 Sprat Sprat 3 Sprat 1,2 20 0,6 0,9 2 15 0,4 0,6 1 10 0,2 0,3 5 0,0 0,0 0 3,00 0,6 18 3,5 16 2,5 0,5 3,0 Plaice Plaice -3 14 Plaice Plaice 0,4 2,5 2,0 12 2,0 0,3 10 1,5 1,5 Y Data Y 0,2 8 1,0 6 1,0 -3 0,1 0,5

n 10 000 m 000 10n 4 0,5 0,0 2 0,0 0,0 0,6 1,00 0,6 1,0 0,5 0,8 0,5 0,8 Sole Sole Sole Sole n 10 000 m 000 10n 0,4 0,6 0,4 0,6 0,3 0,3 0,4 0,4 0,2 0,2 0,2 0,1 0,2 0,1 0,0 0,0 0,0 0,0 1,0 1,0 0,4 0,25 Cod 0,8 Cod 0,8 Cod Cod 0,20 0,3 0,6 0,6 0,15 0,2 0,4 0,4 0,10 0,1 0,2 0,2 0,05 0,0 0,0 0,0 0,00 0,25 Whiting 0,20 0,15 0,10 07:20-09:30 09:20-11:39 11:39-13:49 13:49-16:01 16:01-18:10 18:10-20:20 20:20-22:32 22:32-00:42 00:42-02:54 02:54-05:03 05:03-07:13 07:13-09:22 06:47-08:59 08:59-10:33 10:33-12:43 12:43-14:55 14:55-17:07 17:07-19:19 19:19-21:31 21:31-23:43 23:43-01:52 01:52-04:04 04:04-06:16 06:16-08:28 09:12-11:22 11:22-13:32 13:32-15:41 15:41-17:51 17:51-20:00 20:00-22:12 22:12-00:24 00:24-02:34 02:34-04:46 04:46-06:58 06:58-09:10 09:10-11:20 0,05 0,00 09:35-11:44 11:44-13:54 13:54-16:06 16:06-18:15 18:15-20:27 20:27-22:39 22:39-00:51 00:51-03:03 03:03-05:13 05:13-07:25 07:25-09:35 Catch time

Figure 4: Catch numbers from sampling the cooling water intake over a period of 24-hours (one daily cycle, two tidal cycles). High (HW) and low (LW) water times are given above and are indicated as solid (HW) and dashed (LW) lines in the graphs. For July and August, catch times refer to central european summer time, catch times in October are central european time. During the four 24 h-samplings presented, whiting were only caught in August 2005.

Seabird feeding observations and stow net fishery

Arctic terns were used as representative examples of fish eating seabirds, obviously catching available fish in a way different from the stow net (Fig. 5). The only fish that was observed to be fed to tern chicks and occurred in approximately the same proportions in the stow net catches was Nilsson’s pipefish Syngnathus rostellatus , which acounted for 7-30 % in the net catches and 13-28 % in the tern chicks’ diet. On July 5 th , 11 th and 12 th , herring and sprat together made up 60-80 % of the stow net catches, while they represented only 3-18 % of the food items fed to tern chicks. Interestingly, the proportion of clupeid fish fed to chicks increased substantially between July 20 th and 26th, while herring was not caught at all by the stow net. The only clupeid fish present in the stow net catches were sprat (5 %) and twaite shad Alosa fallax (25 %), the latter not being utilized by the terns as was revealed by analyses of length distributions (not presented here, see Schreiber 2006). While sandeels Ammodytes spec .were not caught by the stow net, 5-18 % of tern chicks’ diet consisted of sandeels. Species with demersal lifestyles, such as gobies ( Pomatoschistus spec .), flatfish and crustaceans (brown shrimp Crangon crangon and common shore crab Carcinus maenas ) were not sampled by the stow net, but were regularly present in tern chicks’ diet in proportions of altogether up to 43 %.

Clupeidae 05.07.2006 Herring and sprat Unknown stow net catches, n = 2907 Goby feeding observations, n = 14 Lesser sandeel Flatfish Nilsson's pipefish others Swimming crab

Clupeidae 11.07.2006 Herring and sprat Common shore crab Brown shrimp stow net catches, n = 9980 Unknown feeding observations, n = 34 Flatfish Lesser sandeel Goby Fish larvae Nilsson's pipefish others

Clupeidae 12.07.2006 Herring and sprat

Goby stow net catches, n = 21810 feeding observations, n = 17 Lesser sandeel Flatfish Fish larvae Nilsson's pipefish others

Smelt 26.07.2006 Brown shrimp Goby stow net catches, n = 13004 Lesser sandeel fedding observations, n = 72 Unknown Flatfish Clupeidae Sprat Nilsson's pipefish Twaite shad Horse mackarel

0 20 40 60 80 % of whole catch

Figure 5: Stow net catches synchronized with observations of prey organisms of Arctic Terns ( Sterna paradisaea ) being fed to chicks on Minsener Oog in July 2006. Stacked bars show herring (black) and sprat (white) shares in stow net catches. Regional fish monitoring programmes

In the Wadden Sea region (extending from , to Skallingen, ) five regular fish surveys are carried out, yielding information on the state of aquatic communities (Tab. 1). The surveys have produced valuable data series on fish and invertebrate abundance, reaching back between 16 (Schleswig-Holstein stow net survey) and 47 years (Fyke net survey, Texel). Three out of these five surveys target demersal fish and invertebrate species, using beam trawls (DYFS, DFS, SNS) to obtain the samples. This type of catching device may also coincidentally catch pelagic species, e. g. when lowering and lifting the net through the water column, yet the only survey that samples pelagic fish quantitavely is the Schleswig-Holstein stow net fishery. Every year in early fall, the demersal surveys are carried out, resulting in a good spatial coverage of the whole Wadden Sea area, except for the Danish part, where no appropriate fish monitoring program has taken place since the 1960s. Seasonal effects as well as tidal and diurnal variability are not considered by these programs due to the emphasis to achieve a good spatial coverage. The other extreme is the Fyke net survey on Texel with an exceptionally high temporal resolution (daily samplings), but only on a few sampling spots. The Schleswig-Holstein stow net survey takes place the first week in August (provided adequate weather conditions), at four stations in the National Park Schleswig-Holsteinisches Wattenmeer, three of which are located in the Meldorf Bight, one in the Hörnum deep south of .

North Sea wide fish monitoring programmes

North Sea wide surveys include the International Bottom Trawl (IBTS), Beam Trawl (IBeamTS) and Herring Larvae (IHLS) Surveys, as well as the Herring Acoustic Survey (HERSUR), the German Small Scale Bottom Trawl Survey (GSBTS) and the Winter Crangon Survey (WCS), having produced data series of 26-35 years using more or less standardized survey design (time, place, gear, Tab. 2). Various groups of target species are anually sampled, but, as with the Wadden Sea surveys, emphasis is placed on demersal species. The only pelagic gears employed are the pelagic trawl used to obtain reference catches for the HERSUR and the GULF III plankton net used in the IHLS. Since it is impossible to obtain fine scale information for the whole North Sea, surveys covering the whole area (see Tab. 2) are supplemented by the GSBTS, which employs the same gear as the IBTS to carry out high intesity sampling in selected areas (12 areas distributed over the whole North Sea, see Ehrich et al. 2007 for details). Again, the data situation for demersal species is far better than for pelagic fish, due to the extensive employment of bottom-trawls.

Common Tern breeding phenology

The course of the breeding season of the terns is subject to an annual variation of approximately two weeks. Factors causing a deviation from the long-term average of events (such as courtship, breeding, chick rearing and fledging) include the weather situation and feeding conditions (Becker 1996). For 2006, the phenological data were collected in the colony in Wilhelmshaven (Tab. 3), where the breeding season is approximately 10 days ahead of other colonies on the Wadden Sea islands coast. From the beginning of May until early July terns are present in the colonies, allowing for studies on their breeding and feeding behaviour potentially supplementing fish survey data (Tab. 3). During the breeding of the terns, no regular fish surveys are carried out (Tabs. 1-3), so fish data are usually not available at that time.

Table 1: Specifications of regular fish survey programmes implemented in the Wadden Sea area.

Survey name Period Temporal scale Spatial scale Gear Target organisms Comments

Schleswig-Holstein 1991-ongoing 1st week in August, North-Frisian Stow net , All fish and Representative for all mobile fish, spatial Stow net survey 1997-2001 June & Wadden Sea, mesh 10 mm invertebrates and temporal coverage low August Meldorf Bight, since in codend 2001 additional station in Hörnum deep

Demersal Young 1974-ongoing 1974-2004 Apr./ May & German Wadden Sea 3 m-Beam trawl Demersal fish, Pelagic species underrepresented Fish Survey (DYFS) Sept./ Oct., 2005- with bobbins, benthic invertebrates temporal coverage low, good spatial ongoing Sept./ Oct. Mesh 20 mm resolution

Demersal Fish Survey 1969-ongoing 1969-1986 spring and Dutch Wadden Sea, 3 m-Beam trawl Demersal fish, See DYFS (DFS) autumn surveys, 1987- Ems-Dollard-Estuary with tickler benthic invertebrates present only autumn chain, mesh survey 20 mm

Sole Net Survey 1974-ongoing 3rd quarter Deeper areas in coastal 7 m-Beam trawl Flatfish, esp. sole & Pelagic and small fish underrepresented, (SNS) zones between mesh 80 mm plaice, invertebrates, good spatial coverage, temporal coverage Belgium and Denmark larger organisms than low DYFS and DFS

Fyke net sampling, 1960-ongoing Mar.-Oct. daily Texel, nearshore Fyke net , All fish and Pelagic species underrepresented, spatial Texel on weekdays mesh 20 mm invertebrates coverage low, very good temporal resolution

Table 2: Specifications of selected regular fish survey programmes implemented in the North Sea area.

Survey name Period Temporal scale Spatial scale Gear Target organisms Comments

International Bottom 1974*-ongoing 1974-1990 1x/ year Entire North Sea Otter trawl All fish, Pelagic fish underrepresented Trawl Survey (IBTS) mostly in Feb., (GOV: mesh invertebrates good spatial coverage, temporal resolution 1991-1996 quartely, 50 mm, MIK low 1997-present 1 st & plankton net) 3rd quarter

International Beam 1985-ongoing Anually, 3 rd quarter Southern & central 7-m- beam-trawl flatfish Pelagic and small fish underrepresented, Trawl Survey (IbeamTS) North Sea mesh 80 mm good spatial coverage, temporal resolution (see SNS) low

North Sea Herring 1984-ongoing Anually 2 nd / 3 rd quarter Entire North Sea Hydroacoustics, Herring, sprat Low temporal resolution, juvenile stages Acoustic Survey Reference catches underrepresented (HERSUR) with pelagic trawl, mesh 20 mm

German Small Scale 1986-ongoing Anually 1 st and 3 rd 1st qu. German Bight, GOV (see IBTS), see IBTS Good temporal coverage, spatial coverage Bottom Trawl Survey quarter, covering 3rd qu. 12 areas (Boxen, 2-m beam trawl, low (GSBTS) = “Boxen” several months 10 x 10 nm) over entire mesh 20 mm North Sea

International Herring 1972-ongoing Anually 1 st and 3 rd English channel, western Pelagic net Gulf North Sea Spatial and temporal coverage sufficient, Larvae Survey (IHLS) quarter North Sea, III, mesh 300 µm autumn spawn. local spawning populations not considered herring larvae

Winter Crangon Survey 1991-ongoing Anually, 1 st quarter German Bight 7-m shrimp trawl, Demersal fish, (WCS) mesh 20 mm invertebrates

*Initiated in 1960/61, 1965 with the participation of the Netherlands named International Young Herring Survey (IYHS), various national surveys followed in the 1980s (English, Scottish and German Ground Fish Surveys), all integrated under the name IBTS in 1990. 1974 marked the starting point of fishery-independent sampling campaigns covering the whole North Sea. Common Tern breeding phenology

Table 3: Common Tern ( Sterna hirundo ) breeding phenology.

Event Time frame 2006* (after Becker & Ludwigs 2004)

Arrival of first terns Mid to end of April April 19th Arrival peak End of April, beginning of May April 21 st (200 Ind.) May 5 th (72 Ind.) First eggs Middle of May May 5 th Egg laying peak Mid May to beginning of June May 15 th , June 2 nd First chicks hatched Beginning to mid June May 31 st Chick peak Middle to end of June June 10 th , June 26 th First chicks fledged End of June to mid July June 28 th Fledging peak Beginning to end of July July 7 th , July 24 th Breakup of colonies Beginning to end of August Last birds leave the colony Mid September September 14 th

* observed at the breeding colony Banter See, Wilhelmshaven, where the breeding season is approximately 10 days ahead of other colonies along the Wadden Sea coast.

DISCUSSION

Fish catches obtained from the cooling water intake of a power plant and a stow net operated on board a commercial fishing vessel in 2006 were analysed with exclusive focus on phenological aspects (seasonal, diurnal and tidal variability) of fish occurrence to derive principles for surveying fish in the Wadden Sea. Marked differences between catches at the three fishing locations as well as a distinct seasonality of abundance of the species examined became evident. The great majority of individuals caught were juveniles, confirming the Wadden Sea to be an important nursery. Abundance peaks were observed mainly before August/ September, when regular survey programmes are usually carried out (Tab. 1). None of the fish sampling programmes tracks the seasonal variability in species abundance, yet important phenomena are likely to be missed, when surveys are restricted to a small time window and/or are of limited areal extent. For example, herring migrated into the Wadden Sea in April, leaving already in the middle of July, suggesting that sampling carried out only in August would most likely have failed to deliver data representative of the state of the population. Moreover, the abundance of herring would have been underestimated if only catches from the Jade Bay were considered. The clear differences in frequency and magnitude of sole catches are another example for the considerable small scale variability characteristic for the Wadden Sea. Other important events may be left undetected by a low temporal and spatial resolution of samplings, such as the spawning of anchovies Engraulis encrasicolus in May/ June 2007 the Jade area or the mass occurrence of whiting in 2007, starting to become evident in early June, dramatically improving the prey availability of piscivorous seabirds, but at the same time diminishing fishermens’ prospects for a profitable catch season due to the whitings’ disposition of heavily preying upon brown shrimp Crangon crangon (Dänhardt and Becker, unpublished). According to our findings, at least quartely fish samplings are needed to account for the observed variability. The great variation of catch numbers both in the course of a day and a tidal cycle requires continuous catches over at least 24 hours (Vorberg 2001), either by using stow nets, or by applying trawled gear repeatedly. However, hauls have to be short if large areas are to be covered by a sampling regime. In this case, large numbers of hauls have to be conducted under similar hydrographical conditions in the tidal or the diurnal period to ensure comparability among samples obtained from different areas. The pronounced differences in catch numbers between stow net and cooling water catches show the limitation of using only one single method to generate data sufficiently close to reality. Thus, in agreement with Hinz (1989), Ruth and Berghahn (1989) and Vorberg et al. (2005), a combination of catch methods is recommended, one of which could be feeding observations in colonies of piscivorous seabirds (Becker et al. 2001b, Harris et al. 2007). In the present study, the catch composition of the stow net was different from that of Arctic terns feeding their chicks on Minsener Oog. This became particularly evident in the share of sandeels, making up almost a fifth of the chicks’ diet, while these fish were not caught at all by the stow net, which usually performed well, at least in terms of quantity (Figs. 1-3) and species number (see also Breckling and Neudecker 1994). The different catchability of the two “fishing methods” stow net and avian piscivore underlines the potential of the latter to deliver valuable supplementary data on fish occurrence: If the terns would not have been observed feeding their chicks, stow net catches alone would not have revealed the presence of sandeels. Besides direct observations of food provisioning rates of tern chicks, we suggest the standardized recording of chick growth rates as a measure sensitive to food variability (Thyen et al. 1998) in seabird colonies representative for local populations (Südbeck et al. 1998), synchronized with surveys of demersal and especially pelagic fish. In all but one Wadden Sea fish survey (the Schleswig-Holstein stow net survey) pelagic fish are underrepresented, and since terns prey upon pelagic fish (Greenstreet et al. 1999), observations of seabird feeding and chick growth rates may improve the fragmentary data situation on pelagic fish (or pelagic stages of demersal fish), which also could be a major source of uncertainty with respect to fish recruitment variability and the output of ecosystem models (e.g. multi- species virtual population analysis for the North Sea), as discussed by Flöter and Temming (2003). Fish surveys in the North Sea outside the Wadden Sea face the challenge of collecting samples representative of a huge area. While programmes like the IBTS cover the whole North Sea at a rather coarse resolution (30 x 30 nautical miles), the GSBTS has been installed to provide high intensity sampling in selected areas, owing to the great variability even for evenly distributed species and between hauls. This strategy has proven successful in interpreting the area-wide data, not at last due to an improved understanding of the effects of spatial scales (Ehrich et al. 2007). For the Wadden Sea, a similar approach may prove reasonable, in that a grid of catch stations with gear both sampling the pelagic and the bottom alike (e. g. a pelagic trawl and a beam trawl, Dänhardt and Becker, unpublished) be established, with a higher temporal resolution of catches close to seabird colonies (Südbeck et al. 1998). In order to fully account for the connectivity of ecosystems, which is a central idea to the ecosystem approach to fisheries management (Marasco et al. 2007), sampling programmes should be harmonized with regard to sampling method, frequency and data analysis. In the North Sea, such efforts have been made for brown shrimp: Winter surveys in January (Tab. 1) have shown that the species occurs not only in the deeper parts off the islands along the coast but must be present also in shallow waters in considerable densities. That was deducted from the observation that sometimes highest catches by RV “Solea” occurred at the shallowest possible stations (~ 9 metres) near the East . Therefore commercial vessels were chartered to fish from the shallowest possible areas to depths where RV “Solea” was able to fish as well to cover the greatest depth range possible, i. e. from 2 metres down to a maximum of 52 metres. An overlap from 9 to 25 metres was possible by almost parallel fishing in the East Frisian region. Parallel application of standard gears used in the local (Tab. 1) and the North Sea wide (Tab. 2) fish surveys following the example outlined above would provide the basis for the link between Wadden Sea and North Sea survey data needed for the practical implementation of the ecosystem approach. For pelagic species, a pelagic trawl comparable to that used for the reference catches in HERSUR (Tab. 2) would have to be newly implemented.

CONCLUSION

The current management strategy for the Wadden Sea exhibits a number of features of the ecosystem approach, such as fixed monitoring objectives for a number of taxa (TMAG 1997), but still leaves room for improvement: - Accounting for their ecological and economic importance as well as the Wadden Sea’s key function as a nursery and transition area in the life history of many migrating species, fish should finally be included in the trilateral monitoring and assessment programme of the Wadden Sea. - Fish surveys should be representative for both demersal and pelagic species and the spatial and temporal resolution of samplings should account for the phenology of species. - Fish-eating seabirds such as terns should be used as indicators of their prey fish populations that mainly consist of pelagic species, which are underrepresented in local and North Sea wide survey programmes. - Local and North Sea wide surveys should be methodically harmonized to account for ecosystem connectivity. The examination of the interannual variability from 2005 to 2007 of seasonal phenomena will be dealt with in detail in a future article and may further complete the understanding of ecosystem functions, thereby improving the calibration of survey programmes to the natural conditions.

ACKNOWLEDGEMENTS

We thank captain K.-H. Rostek for making available his stow net cutter, even at sometimes very short notice. We are grateful to J. Schreiber for his effort to observe Arctic tern chick feeding on Minsener Oog and to K. Wiethölter for her assistence with the cooling water sampling in 2005. The great support from the staff at the E.on power plant in Wilhelmshaven is much appreciated. Financial support for this project was provided by the Niedersächsische Wattenmeerstiftung, No 53-NWS-41/04.

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