Journal of Fish Biology (2015) 87, 449–464 doi:10.1111/jfb.12731, available online at wileyonlinelibrary.com

Spatial ecology of coastal Atlantic cod Gadus morhua associated with parasite load I. M. Aalvik*†, E. Moland†‡§, E. M. Olsen*†‡ and N. C. Stenseth*†‡ *Centre for Ecological and Evolutionary Syntheses (CEES), Department of Biosciences, University of Oslo, P. O. Box 1066 Blindern, N-0316, Oslo, Norway, †Institute of Marine Research, Flødevigen Marine Research Station, Nye Flødevigveien 20, N-4817, His, Norway and ‡Centre for Coastal Research, Department of Natural Sciences, University of Agder, P. O. Box 422, N-4604, Kristiansand, Norway (Received 9 November 2014, Accepted 22 May 2015) Acoustic tags and receivers were used to investigate the spatial ecology of coastal Atlantic cod Gadus morhua (n = 32, mean fork length: 50 cm, range: 33–80 cm) on the Norwegian Skagerrak coast in 2012. Monthly home ranges (HR), swimming activity and depth use varied considerably among individuals and through the months of June, July and August. HR sizes for the period ranged from 0⋅25 to 5⋅20 km2 (mean = 2⋅30 km2 ). Two thirds of the tagged G. morhua were infected with black spot disease Cryptocotyle lingua parasites; these fish had larger HRs and occupied deeper water compared with non-infected fish. The infected fish also tended to be more active in terms of horizontal swimming. From an ecological and evolutionary perspective, any environmental change that modifies G. morhua behaviour may therefore also alter the parasite load of the population, and its conservation and fishery status. © 2015 The Fisheries Society of the British Isles

Key words: acoustic telemetry; black spot disease; Cryptocotyle lingua; home range; life-history traits; local populations.

INTRODUCTION Obtaining knowledge on fine-scale ecology and behaviour that underlie observed movement patterns in fishes is vital for sustainably managing the species in question. Fishes may exhibit high interindividual variation in behaviour that is maintained through time and across contexts and therefore can be defined as personality traits (Olsen et al., 2012; Wolf & Weissing, 2012). More broadly, such individual behaviours may represent part of a pace-of-life syndrome, where behavioural traits are coevolving with a range of life-history and physiological traits (Réale et al., 2010). For instance, theory predicts that a typical slow pace-of-life is characterized by low individual growth rate, low dispersal and activity level and high immunocompetence (Réale et al., 2010). Individual variation in behaviour can be influenced by numerous biotic and abiotic factors, where one such factor is the presence and abundance of parasites (Thomas et al., 2005; Poulin, 2010; Hammond-Tooke et al., 2012). From a pace-of-life §Author to whom correspondence should be addressed to permanent address Institute of Marine Research, Nye Flødevigveien 20, 4817 His, Norway. Tel.: +61 7 4781 4111; email: [email protected]

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perspective, an association between behaviour and parasite infection could be caused by (1) certain behaviours increasing the probability of encountering parasites, and (2) evolutionary trade-offs between behaviour and immunocompetence (Réale et al., 2010). Host–parasite interactions are common in the marine environment where, amongst others, fishes serve as hosts to a wide range of taxonomically diverse parasites. Some recognized infection-associated behavioural alterations include and involve, for example, habitat selection, predator–prey interactions, swimming performance, mate choice and foraging efficiency (Barber et al., 2000; Olsen et al., 2000). Atlantic cod Gadus morhua L. 1758 stands out for being a host to an extensive diversity of parasites, stemming from the fish’s omnivorous diet and vast geographical distribution, while at the same time being preyed upon by a number (and diversity) of organisms and thus can be used as intermediate as well as definitive host (Hemmingsen & MacKenzie, 2001). Recent studies have shown that mobile species such as G. morhua can be structured into local populations on a surprisingly small scale (Knutsen et al., 2003; Jorde et al., 2007). Management needs to acknowledge this fine-scale population diversity because it can be important for the overall resilience of the population complex (Loreau et al., 2001; Conover et al., 2006; Hutchings et al., 2012). Further, the depleted status of many G. morhua stocks combined with high ensuing fishing pressure calls for management actions to ensure viable populations and fisheries into the future (Wroblewski et al., 2005). In order to implement such a sustainable management approach, more information on coastal G. morhua’s spatial ecology is required. For this purpose, acoustic telemetry has become a widely recognized tool (Heupel & Simpfendorfer, 2002; Heupel et al., 2006). Acoustic telemetry is appropriate as a monitoring technology as long as the animal is sufficiently large to have a transmitter attached or implanted, without influencing the animal’s behaviour or quality of life (Heupel et al., 2006). This monitoring method enables observation of fine-scale movements of each tagged animal, as the acoustic tag transmits a unique signal that is picked up by a network of moored receiver stations. By using acoustic telemetry, the objective of this study was to obtain new knowledge on fine-scale spatial ecology of coastal G. morhua on the Skagerrak coast of southern Norway and to quantify behavioural traits underlying the movement patterns observed. Based on the general predictions from life-history theory, it was hypothesized that behavioural traits of individual G. morhua would co-vary with physiology (parasite load) and life history (juvenile growth, age and body size).

MATERIALS AND METHODS S T U DY S Y S T E M This study was conducted within a 5 km2 area on the Norwegian Skagerrak coast during 2012 (Fig. 1). The study area is a semi-sheltered embayment located 1–5 km south-west of the Institute of Marine Research (IMR) Flødevigen marine research station. The area includes numerous islands and islets and has a maximum depth of c. 40 m along the eastern perimeter of the hydrophone receiver array. The dominant substratum type between 5 and 10 m depth is hard bottom and macro-algae habitats that are important feeding habitats for coastal predators such as G. morhua (Hop et al., 1992; Espeland et al., 2010; Olsen et al., 2012). Within basins and flat areas, the substratum is dominated by sand or mud with patches of eel grass that function as nursery areas for G. morhua (Gotceitas et al., 1997; Fromentin et al., 1998). There is freshwater discharge from the River Nidelva into the northern part of the study area.

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Fig. 1. (a) The study area (Sømskilen) with 5, 10, 15, 20, 30, 40, 100 and 150 m depth contours; , position of acoustic receivers (n = 44). (b) Location of the study area on the Norwegian Skagerrak coast; inset: the Scandinavian Peninsula (Norway and Sweden), Denmark and the location of the Skagerrak Sea.

S T U DY S P E C I E S Gadus morhua is found in both coastal waters and offshore shelf habitats, distributed in the eastern and western North Atlantic Ocean, where fish located along the Norwegian Skagerrak coast form a network of biologically distinct local populations (Knutsen et al., 2003; Jorde et al., 2007; Olsen et al., 2010). Fishing mortality can be as high as 50% per year within these coastal populations (Olsen & Moland, 2011), and few individuals survive beyond age 5 or 6 years (Olsen et al., 2004). The Skagerrak coastal populations have experienced a long-term decline in abundance and phenotypic diversity (Svedäng & Bardon, 2003; Olsen et al., 2009), which is probably caused by multiple drivers including harvesting, climate change and ecosystem regime shifts (Olsen & Moland, 2011; Rogers et al., 2011; Johannessen, 2014). Gadus morhua is an exceedingly fecund broadcast spawning species (Kjesbu, 1989). In coastal Skagerrak, spawning typically occurs in sheltered fjord basins during January to April (Espeland et al., 2007; Ciannelli et al., 2010). Coastal G. morhua in Skagerrak typically grow 10–15 cm per year and mature when they are 2–3 years old (Olsen et al., 2008). The minimum legal size for harvesting G. morhua in this region is 40 cm fork length (LF ). The Skagerrak coastal fish is harvested using a wide variety of gear including bottom trawl, gillnet, longline, seine, traps and hand line (Julliard et al., 2001). Gadus morhua are hosts to a rich and diverse parasitic community (107 taxa from 10 phyla) that varies seasonally, with locality and depending on the age and size of the fish, where the predominant parasitic groups are trematodes and nematodes (Hemmingsen & MacKenzie, 2001; Perdiguero-Alonso et al., 2008). A C O U S T I C T E L E M E T RY To monitor fish movement, a system of moored acoustic receivers (VR2W, Vemco Divison, Amirix Systems Inc.; www.vemco.com) was used. The receivers (n = 44) are distributed all throughout the study area (Fig. 1), attached to subsurface buoys anchored to the seabed and positioned 3 m below the surface. The receivers were distributed to ensure overlapping detection ranges, confirmed by a recent range-testing study (Olsen & Moland, 2011). The receivers’ record of presence or absence information on tagged G. morhua within the study area was used to estimate fish movement traits.

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S A M P L I N G P ROTO C O L Gadus morhua were captured using fyke nets soaked for 1–6 days. A total of 80 individuals were selected for acoustic tagging according to length and capture location, where the aim was to sample roughly an equal number of fish throughout the available size range and area of capture. All 80 G. morhua were also tagged with an external T-bar anchor tag (TBA-2, Hallprint Pty. Ltd; www.hallprint.com) by the first dorsal fin. The external tags were used in addition to the acoustic tags to maximize information about harvested fish, having a unique identification number along with contact information (the address of IMR Flødevigen) and posting a high reward of 500 NOK (c. $63 U.S.) for tag returns. Tagged fish were equipped with a V9P-2L transmitter (9 mm × 38 mm, 0⋅8) and thus not included as explanatory variables. The main focus of this study was to quantify how LF (in addition to parasites) could influence fish behaviour. Specifically, the model selection philosophy of Burnham & Anderson (2002) was adopted for making inferences about the sampled population, emphasizing a careful selection of a priori candidate models rather than exploring all combinations of available variables. Fish identity was set as the random factor; when random factor is specified, the randomness inherent in the data (repeated observations of individuals) is accounted for and so overcomes pseudoreplication (Millar & Anderson, 2004). Both top-down and step-up manual model selections were performed by comparing Akaike information criteria (AIK) values of a set of a priori selected candidate models (Burnham & Anderson, 2002). AIC provides an estimate of model suitability based on a trade-off between goodness of fit and model complexity and parsimony (number of parameters included, addition of parameters penalizes model AIC) (Bozdogan, 2000). By using second-order AIC (AICc ), a small sample size (n = 32) is corrected for (Hurvich & Tsai, 1989; Burnham & Anderson, 2002). When comparing models, the simplistic measure 𝛥AICc was employed, which allowed each model relative to the best model to be evaluated and when 𝛥AICc is > 2 the model is said to have substantial evidence for its validation (Burnham & Anderson, 2002). Models were fitted using maximum likelihood (ML) estimation via the lme function in the R library nlme (Pinheiro & Bates, 2000).

RESULTS During the 3 month study period, nine G. morhua were found to be dead by natural causes, 13 were harvested, 17 dispersed out of the study area (either permanently or temporarily during the 3 month study period) and nine tags malfunctioned. The tagged fish for which movement traits (n = 32) were analysed ranged from 33 to 80 cm (mean = 50 cm) LF , from 0⋅34 to 4⋅76 kg (mean = 1⋅37 kg) in mass and from 2 to 6 years (mean = 3⋅4 years) in age. Backcalculated LF at year one (L1 ) ranged from 9 to 26 cm (mean = 15⋅6 cm). The most abundant parasite found was C. lingua, with 81% of the fish being infected. In addition, a total of 21% of the fish were infected with L. branchialis and 59% were infected with C. elongates. Total HR size (95% kernel UD) varied substantially among individuals (Table I), from 0⋅25 to 5⋅20 km2 for the whole study period (mean = 2⋅3 km2 ). Monthly HRs

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also varied considerably among individuals (Fig. 3) and tended to be larger in August (mean ± s.d. = 1⋅25 ± 1⋅24 km2 ), compared with June (0⋅55 ± 0⋅43 km2 ) and July (0⋅42 ± 0⋅23 km2 ). Cumulative distance travelled by individual G. morhua ranged from 15⋅2 to 78⋅8 km for the whole study period (mean = 42⋅4 km). Cumulative distance travelled also tended to be larger in August (mean ± s.d. = 16⋅9 ± 7⋅9 km) compared with June (12⋅4 ± 4⋅9 km) and July (13⋅1 ± 6⋅1 km). The depth used by G. morhua throughout the study period ranged from 0⋅0 to 45⋅7 m (mean = 12⋅4 m). Gadus morhua used somewhat deeper waters in August (mean ± s.d. = 14⋅8 ± 4⋅8 m) compared with June (10⋅6 m ± 3⋅3 m) and July (12⋅3 ± 3⋅8 m). LME models supported effects of month, juvenile growth (i.e. backcalculated LF at age 1 year) and presence of the C. lingua parasite on (1) HR, (2) cumulative distance travelled and (3) mean depth used (Table II). Simpler models, as well as more complex models including observed LF and the presence of the parasites L. branchialis and C. elongates, received less support (𝛥AICc < 2). Although included in the best models, juvenile growth had only marginal effects on all the three behavioural traits (Table II). The presence of C. lingua was associated with larger HRs, larger mean depth and larger cumulative distances moved compared with un-infected fish (Table II).

DISCUSSION This study found a positive association between individual behaviour, quantified as HR size, distance travelled and depth use and infection by the ectoparasite C. lingua. These results are discussed against general theoretical predictions from life-history and behavioural theory and also from a management and conservation perspective. Although the underlying mechanism is not determined by the study, it is likely that more active G. morhua are also more prone to infection due to a more bold and exploratory behaviour which may in turn expose such individuals to areas with elevated densities of C. lingua cercariae. Snails in the tidal zone, mainly the littoral winkle Littorina littorea act as the first intermediate host, releasing cercariae that infect several species of fishes as the second intermediate host. Piscivorous birds (often gulls) and mammals act as the parasite’s definitive hosts (Stunkard, 1930; Lysne et al., 1998). Cercariae of C. lingua display positive phototaxis (Stunkard, 1930) and alternate between bursts of vertical swimming and sinking (Rea & Irwin, 1995). In a field experiment, Lysne et al. (1998) found that caged G. morhua kept at 0–2 m depth accumulated significantly more parasites than those kept at 2–4 m during a 6 month period, and that distance from shore did not affect infection rates. If the more active fish in this study were those exhibiting longer cumulative distances, resulting in larger HRs or higher within-HR activity, and if this reflects their behaviour in the past, these individuals might also have been more exposed to habitats where cercariae density was elevated. The data, however, did not suggest that infected fish spent more time in shallow water, which is likely to harbour such habitats. As data are lacking on behaviour during time of infection, the effect of a more active behaviour on infection risk can only be speculated on. Alternatively, the parasite might be affecting the behaviour of the fish directly or indirectly via changes in the energy budget, stamina or general health of the fish (Thomas et al., 2005). Some parasites are capable of manipulating the behaviour of their hosts by affecting brain functions. A well known example is the trematode Dicrocoelium dendriticum

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Table I. Behavioural estimates for the 32 Gadus morhua included in the study ID 7288 7288 7288 7293 7293 7293 7294 7294 7294 7303 7303 7303 7305 7305 7305 7306 7306 7306 7307 7307 7307 7308 7308 7308 7309 7309 7309 7312 7312 7312 7320 7320 7320 7321 7321 7321 7326 7326 7326 7327 7327 7327 7330 7330 7330 7334 7334 7334

HR Mean Cum. Month depth (m) dist. (km) (km2 ) 6 7 8 6 7 8 6 7 8 6 7 8 6 7 8 6 7 8 6 7 8 6 7 8 6 7 8 6 7 8 6 7 8 6 7 8 6 7 8 6 7 8 6 7 8 6 7 8

10⋅73 12⋅20 13⋅56 10⋅71 13⋅59 14⋅20 8⋅46 8⋅90 16⋅02 11⋅47 13⋅08 16⋅54 8⋅77 20⋅41 22⋅20 13⋅30 15⋅77 19⋅41 8⋅20 8⋅26 10⋅08 14⋅13 14⋅73 18⋅59 11⋅26 10⋅89 9⋅01 14⋅17 16⋅43 13⋅59 6⋅73 14⋅27 14⋅09 5⋅96 5⋅91 5⋅83 6⋅87 6⋅68 7⋅54 14⋅53 11⋅79 14⋅20 9⋅24 9⋅70 12⋅31 7⋅44 10⋅71 21⋅65

11⋅13 12⋅51 15⋅16 14⋅61 13⋅79 19⋅27 8⋅90 6⋅99 17⋅23 7⋅23 4⋅02 3⋅98 22⋅95 10⋅87 12⋅40 21⋅84 27⋅82 29⋅12 19⋅44 18⋅44 10⋅68 13⋅20 17⋅99 32⋅17 20⋅22 18⋅78 23⋅33 12⋅18 6⋅99 8⋅49 13⋅03 13⋅28 17⋅36 16⋅13 11⋅28 17⋅56 6⋅62 7⋅20 3⋅96 15⋅41 19⋅25 21⋅55 14⋅11 8⋅57 11⋅97 12⋅48 21⋅06 31⋅83

1⋅87 0⋅64 2⋅69 0⋅80 0⋅68 0⋅40 0⋅48 0⋅37 1⋅25 0⋅33 0⋅26 0⋅30 0⋅65 1⋅01 1⋅10 0⋅41 0⋅53 1⋅12 0⋅28 0⋅21 0⋅21 0⋅57 0⋅54 0⋅26 0⋅39 0⋅25 0⋅48 1⋅35 0⋅29 0⋅92 0⋅25 0⋅15 3⋅25 0⋅25 0⋅19 0⋅11 0⋅34 0⋅30 0⋅94 1⋅40 0⋅71 0⋅45 0⋅31 0⋅19 2⋅92 0⋅48 0⋅40 2⋅10

ID 7336 7336 7336 7339 7339 7339 7341 7341 7341 7342 7342 7342 7343 7343 7343 7345 7345 7345 7346 7346 7346 7349 7349 7349 7353 7353 7353 7356 7356 7356 7357 7357 7357 7358 7358 7358 7359 7359 7359 7360 7360 7360 7363 7363 7363 7364 7364 7364

HR Mean Cum. Month depth (m) dist. (km) (km2 ) 6 7 8 6 7 8 6 7 8 6 7 8 6 7 8 6 7 8 6 7 8 6 7 8 6 7 8 6 7 8 6 7 8 6 7 8 6 7 8 6 7 8 6 7 8 6 7 8

12⋅58 13⋅94 18⋅05 9⋅31 9⋅80 14⋅86 14⋅53 13⋅12 10⋅41 5⋅34 5⋅09 5⋅47 9⋅12 10⋅05 12⋅50 4⋅98 7⋅36 11⋅55 11⋅62 12⋅96 16⋅95 8⋅21 9⋅62 15⋅43 13⋅24 14⋅71 15⋅24 13⋅99 13⋅72 14⋅52 16⋅23 14⋅70 20⋅98 9⋅84 20⋅11 21⋅79 7⋅45 8⋅71 11⋅07 10⋅68 14⋅01 25⋅82 12⋅90 13⋅85 14⋅38 17⋅56 17⋅32 16⋅54

17⋅23 27⋅23 21⋅73 7⋅52 8⋅35 21⋅67 12⋅10 11⋅98 9⋅82 14⋅43 16⋅88 6⋅06 13⋅07 19⋅99 22⋅70 4⋅18 6⋅43 12⋅10 11⋅40 10⋅97 15⋅59 19⋅47 17⋅96 17⋅73 7⋅21 7⋅21 8⋅92 7⋅95 15⋅17 32⋅15 8⋅03 10⋅94 17⋅38 7⋅59 6⋅43 10⋅63 8⋅84 6⋅55 12⋅73 11⋅13 12⋅93 26⋅53 11⋅58 13⋅06 18⋅79 5⋅86 7⋅49 10⋅63

1⋅06 0⋅77 0⋅73 0⋅42 0⋅50 4⋅82 0⋅27 0⋅51 4⋅60 0⋅40 0⋅18 0⋅41 0⋅31 0⋅24 0⋅67 0⋅14 0⋅70 0⋅66 1⋅44 0⋅35 0⋅98 0⋅28 0⋅22 1⋅89 0⋅32 0⋅27 0⋅22 0⋅23 0⋅32 0⋅17 0⋅17 0⋅48 0⋅33 0⋅26 0⋅09 0⋅13 0⋅46 0⋅34 1⋅94 0⋅33 0⋅33 1⋅96 0⋅39 0⋅42 1⋅26 0⋅91 0⋅95 0⋅90

ID, telemetry tag identification number for each fish; 6, June; 7 July; 8, August; Cum. dist., cumulative distance; HR, home range size.

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Fig. 3. Home range estimates (95% kernel utilization distribution) of individual Gadus morhua (n = 32) during June, July and August 2012, estimated from acoustic monitoring (see also Fig. 1). Numbers refer to fish ID (see Table I). Colour denotes monthly behaviour: , June; , July; , August.

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Table II. Results of linear mixed-effect models examining behavioural traits of Gadus morhua in relation to month, fork length at year one (L1 ) and parasitic infections. Cod ID was a random effect in the model. Response variables were ln transformed. The Cryptocotyle lingua effect represents presence of parasite, where absence is included in the intercept, along with the month June. Only results from 𝛥AICc = 0 model are shown here 95% c.i. Response

Variable

Estimate

Lower

Upper

P

Cumulative distance

Intercept July August L1 C. lingua Intercept July August L1 C. lingua Intercept July August L1 C. lingua

2⋅796 0⋅134 0⋅361 −0⋅003 0⋅256 0⋅941 0⋅092 0⋅249 0⋅001 0⋅267 13⋅071 −0⋅287 0⋅374 −0⋅002 0⋅514

2⋅074 −0⋅055 0⋅171 −0⋅007 −0⋅109 1⋅513 −0⋅024 0⋅133 −0⋅001 0⋅024 12⋅217 −0⋅606 0⋅056 −0⋅007 0⋅087

3⋅518 0⋅323 0⋅550 0⋅001 0⋅621 2⋅473 0⋅209 0⋅365 0⋅004 0⋅510 13⋅926 0⋅032 0⋅693 0⋅003 0⋅941

>0⋅05 >0⋅05 0⋅05 >0⋅05 >0⋅05 >0⋅05 0⋅05 0⋅05 >0⋅05 0⋅05

Spatial ecology of coastal Atlantic cod Gadus morhua associated with parasite load.

Acoustic tags and receivers were used to investigate the spatial ecology of coastal Atlantic cod Gadus morhua (n = 32, mean fork length: 50 cm, range:...
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