Intraguild predation between small pelagic fish in the ...

Intraguild predation between small pelagic fish in the Bay of Biscay: impact on anchovy (Engraulis encrasicolus L.) egg mortality Eneko Bachiller, Unai Cotano, Leire Ibaibarriaga, Maria Santos & Xabier Irigoien Marine Biology International Journal on Life in Oceans and Coastal Waters ISSN 0025-3162 Volume 162 Number 6 Mar Biol (2015) 162:1351-1369 DOI 10.1007/s00227-015-2674-0

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Author's personal copy Mar Biol (2015) 162:1351–1369 DOI 10.1007/s00227-015-2674-0

ORIGINAL PAPER

Intraguild predation between small pelagic fish in the Bay of Biscay: impact on anchovy (Engraulis encrasicolus L.) egg mortality Eneko Bachiller1,2 · Unai Cotano1 · Leire Ibaibarriaga1 · Maria Santos1 · Xabier Irigoien1,3

Received: 7 November 2014 / Accepted: 27 April 2015 / Published online: 12 May 2015 © Springer-Verlag Berlin Heidelberg 2015

Abstract Small pelagic fish can play an important role in various ecosystems linking lower and upper trophic levels. Among the factor behind the observed inter-annual variations in small pelagic fish abundance, intra- and interspecific trophic interactions could have a strong impact on the recruitment variability (e.g. anchovy). Egg cannibalism observed in anchovies has been postulated to be a mechanism that determines the upper limit of the population density and self-regulates the population abundance of the species. On the other hand, predation by other guild species is commonly considered as a regulation mechanism between competing species. This study provides empirical evidence of anchovy cannibalism and predation of the main small pelagic fish species on anchovy eggs and estimates the effect of intraguild predation on the anchovy egg mortality rate. Results show that, depending on the year (2008– 2009), up to 33 % of the total anchovy egg mortality was the result of sardine predation and up to 4 % was the result of egg cannibalism together with predation by Atlantic and Atlantic Chub mackerel and sprat. Results also indicate that in the Bay of Biscay, fluctuations in the survival index of Communicated by M. Peck. * Eneko Bachiller [email protected] 1

Marine Research Division, AZTI Foundation, Herrera Kaia Portualdea z/g, 20110 Pasaia, Gipuzkoa (Basque Country), Spain

2

Present Address: Pelagic Fish Research Group, Institute of Marine Research (IMR), Nordnes 33, PO box 1870, 5817 Bergen, Norway

3

Present Address: Red Sea Research Center, King Abdullah University of Science and Technology (KAUST), Thuwal 23955‑6900, Saudi Arabia

the early life stages of anchovy are likely to be attributable at least in part to egg cannibalism and especially to a high sardine predation on anchovy eggs.

Introduction The Bay of Biscay is an open oceanic bay with the Spanish coast in the southern part, oriented west to east (the Cantabrian Sea) and the French coast in the eastern part, oriented south to north (Fig. 1). The European anchovy (Engraulis encrasicolus) and sardine (Sardina pilchardus) play central roles in the Bay of Biscay and Cantabrian Sea ecosystems, where, together with other small pelagic species (e.g. Trachurus trachurus, Scomber scombrus), they have been, until recently, commercially exploited (Uriarte et al. 1996; Sánchez and Olaso 2004; ICES 2011a). The closure of the anchovy fishery during the last decade due to a long period of continuously low recruitment (ICES 2008) increased the need to understand processes involving survival of the anchovy’s early life stages and fluctuations between different small pelagic fish stocks in the area. From a wider perspective, various hypotheses to explain inter-annual and long-term variations in small pelagic fish abundance across the world have been proposed. These variations are generally summarized by Bakun’s (1993) triad of retention, production and concentration in relation to mechanisms that limit the dispersion of fish in their early life stages and increase growth rates through expanded production and food concentration. These mechanisms reduce fish mortality in early life stages and improve recruitment. However, Bakun’s triad does not always explain variations in recruitment. As an example, it is difficult to explain the large inter-annual and inter-decadal fluctuations in the abundance of anchovy and sardines in large upwelling

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Fig. 1 Anchovy egg abundance (abd. m−2) distribution observed in the Bay of Biscay during a BIOMAN 2008 and b BIOMAN 2009 surveys. Plankton sampling stations are indicated with small crosses

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systems based on the triad of retention, production and concentration (Baumgartner et al. 1992; Schwartzlose et al. 1999; Chavez et al. 2003). Various factors, such as water temperature or changes in the size of food, have been proposed as causes (van der Lingen et al. 2006, 2009; Takasuka et al. 2007). Anchovy recruitment in the Bay of Biscay has been attributed to upwelling intensity (Borja et al. 1996, 1998; Allain et al. 2001), although the mechanism underlying anchovy recruitment continues to be debated because primary production in the Bay of Biscay is closely related to river discharge, whereas upwelling contributes to larval dispersion (e.g. Cotano et al. 2008; Irigoien et al. 2008). Another possible factor essential to understanding the survival of the anchovy population is the species’ egg mortality index. In the Bay of Biscay, the anchovy’s spawning area is well known because annual evaluation of the biomass has been carried out since 1988 using the daily egg production method (DEPM) (Somarakis et al. 2002, 2004). During last two decades, the DEPM surveys in the Bay of Biscay, such as BIOMAN (ICES 2011a), have provided platform means to sample both zooplankton (including anchovy eggs) and additional fish samples (anchovy adults and other small pelagic species). The abundance and distribution of anchovy eggs have been studied at high spatial resolution during the anchovy’s spawning season (Motos et al. 2005). The main spawning areas have been defined as the Gironde river plume, the Adour river plume and some areas of the shelf break (Motos et al. 1996). In addition, natural egg mortality has been estimated yearly over a long period (e.g. ICES 2011a). However, other than the bottom-up and dispersions mechanisms, the role of predator–prey interactions is a major topic of discussion in fisheries research. Irigoien et al. (2007) proposed that anchovy recruitment over the shelf area in the Bay of Biscay could be controlled by the predation of other pelagic fish on anchovies in their early life stages. Although it has been established that small pelagic species (e.g. anchovy) play a role as forage fish for larger predators such as tuna (Goñi et al. 2011), the potential impact of predation by small pelagic fish on anchovies in their early life stages has not been estimated in the Bay of Biscay. In other locations, egg cannibalism among anchovies has been described as a population density mechanism (Ricker 1958, 1973; Hunter and Kimbrell 1980; MacCall 1981; Alheit 1987; Valdés et al. 1987) and as means to selfregulate population abundance (Valdés Szeinfeld 1991). In fact, among the causes of anchovy egg mortality, egg cannibalism has been reported in several engraulidae populations such as the Japanese anchovy, E. japonicus (Hayasi 1967), the Peruvian anchovy, E. ringens (De Mendiola 1969; Santander et al. 1983; Alheit 1987), the northern anchovy, E. mordax (Loukashkin 1970; Hunter and Kimbrell 1980;

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MacCall 1981), the South African anchovy, E. capensis/ encrasicolus (Valdés et al. 1987; Valdés Szeinfeld 1991) and the Argentine anchovy, E. anchoita (Ciechomski 1967; Pájaro 1993, 1998; Pájaro and Ciechomski 1996; Pájaro et al. 2007; Padovani et al. 2011). Among the European anchovy (E. encrasicolus), cannibalism was observed in the Bay of Biscay (Plounevez and Champalbert 1999) but not in the Mediterranean Sea (Tudela and Palomera 1997; Plounevez and Champalbert 2000). Beyond egg cannibalism, predation by other guild species is commonly considered as a regulation mechanism between competing species (Fox 1975). Most eggs and early larvae of pelagic fish are planktonic and are therefore potential prey for planktivorous fish that compete for food with the parents of the eggs and larvae (Valdés Szeinfeld 1991; Garrido et al. 2008). Clupeiformes are important predators of fish eggs because they are abundant and travel in large schools (Hunter and Kimbrell 1980). Valdés Szeinfeld (1991) estimated that in the Benguela system, 56 % of anchovy egg mortality was attributed to predation by sardines, whereas 6 % was attributed to egg cannibalism by anchovies. Irigoien and De Roos (2011) noted the importance of understanding the effects of intraguild predation in the context of an ecosystem approach to fisheries management because it could influence environmental and fisheries effects. Accordingly, studying anchovy egg predation by small pelagic fish in the Bay of Biscay could contribute to our understanding of the life stages of this species. An egg consumption estimation equation, C = EE gt, has been used previously by several authors (e.g. Santander et al. 1983; Alheit 1987; Valdés et al. 1987; Valdés Szeinfeld 1991; Pájaro et al. 2007), where EE is the mean number of eggs ingested per kg of fish, g is the gastric evacuation rate, and t is the duration of feeding. Previous calculations were performed on other systems and to determine anchovy cannibalism (Santander et al. 1983; Alheit 1987; Valdés Szeinfeld 1991; Pájaro et al. 2007) and predation by sardines (Valdés Szeinfeld 1991) but not on predation by other species. To calculate predation of anchovy eggs by other species, several assumptions are therefore required. These assumptions include: 1. The weighing method applied in the equation. Previous studies did not weight the mean egg consumption by the amount of fish caught at each sampling station. Some considered all sampled fish together (Santander et al. 1983; Alheit 1987; Valdés et al. 1987), whereas others considered the mean egg consumption per sampling station (Valdés Szeinfeld 1991; Pájaro et al. 2007). Further, no previous study considered the sampling effort (i.e. the catch-per-unit-effort, cpue) per station. This measure could be used to consider the

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individual variability observed in stomach contents between sampling hauls (Bachiller 2012), because a single stomach with high egg content could distort the final overall consumption estimation. In the same way, considering the trawling time in the weighting would also allow a better estimation of the predator distribution, given that the fishing effort could affect the total amount of fish caught in each of the landings representative of an extended area (e.g. the area of distribution of anchovy eggs in the Bay of Biscay). 2. Estimation of the gastric evacuation rates in the field (e.g. no feeding takes place during the designated nonfeeding period, captured fish have the same feeding history, and temperature conditions do not change over the 24-h cycle) (Bernreuther et al. 2008). In addition, the gastric evacuation rate in fish is known to be affected by a variety of factors, including prey type and size, meal type, predator type and temperature (for a review, see Bromley 1994), as well as by the time of the day (Nikolioudakis et al. 2011). Previous literature on evacuation rates is scarce and mainly based on single species studies (Tudela and Palomera 1995 for anchovy; Nikolioudakis et al. 2011 for sardine; Dahl and Kirkegaard 1987 for Atlantic horse mackerel; Darbyson et al. 2003 for Atlantic mackerel; Bernreuther et al. 2009 for sprat), addressing previous aspects (assumptions) depending on the biology of each species. Therefore, the use of published gastric evacuation rates implies making the same assumptions for the overall anchovy egg consumption estimation by those species from which information is available (i.e. anchovy, sardine, Atlantic horse mackerel, Atlantic mackerel and sprat). In case of other species sharing the same niche with the anchovy (Bachiller 2012) in the Bay of Biscay (e.g. Mediterranean horse mackerel, Atlantic chub mackerel, bogue), gastric evacuation rates assigned to the closest taxonomic level could be used as a proxy (e.g. using the same rate for both horse mackerel species). 3. A 24-h feeding period for anchovies and sardines (Santander et al. 1983; Alheit 1987; Valdés Szeinfeld 1991). This assumption remains a point of discussion as results for the species in the Bay of Biscay indicate high individual variability in stomach contents, suggesting higher feeding activity during the day (Dahl and Kirkegaard 1986; James and Findlay 1989; Tudela and Palomera 1995; Olaso et al. 1998; Plounevez and Champalbert 1999, 2000; Darbyson et al. 2003; Garrido et al. 2007; Bernreuther et al. 2009; Plirú et al. 2012). On the contrary, other studies report night feeding activity (Gennotte et al. 2007; Nikolioudakis et al. 2011), which can be expected from filter feeders. It is therefore difficult to make an accurate estimation of the feeding period, moreover, considering differences on

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the feeding behaviour depending on the species (e.g. filter feeding by sardine, Nikolioudakis et al. 2011; particulate feeding by horse mackerel, Bachiller and Irigoien 2013). Accordingly, although assuming a 12-h feeding period might be more accurate, comparisons between results obtained following the same methodology as in previous studies (i.e. a 24-h feeding period) should be considered. 4. The total predator biomass. In this sense, previously cited studies have used acoustic estimations for the total area of sampling, and therefore, assuming the total biomass as in previous studies would make new consumption estimations comparable to them. However, targeted predator sampling in the area of distribution of anchovy eggs would be more appropriate. Although this is something difficult to achieve in the Bay of Biscay for all predator species, since stock assessment surveys are focused on the whole distribution area of the species (e.g. ICES 2011a), DEPM surveys allow for an approach constrained to the specific area of distribution of anchovy eggs in case of anchovy and sardine (i.e. considering spawning stock biomass of anchovy, and sardine biomass assuming the same area). This approach would be more accurate for at least these species. However, these results should be compared with consumption estimations based on the total biomass from acoustic estimations (which allow making comparisons between most predator species) and treated carefully, since each sampling effort is biased by its methodology. In this case, trawls are focused on the anchovy spawning period and are not representative of non-spawning anchovy (they would be potential egg predators especially during daytime) or other species (e.g. sardine) distribution. This study proposes a modification to the anchovy egg consumption equation used in the previous literature to estimate the anchovy egg mortality rate due to predation by small pelagic fish, including anchovy cannibalism, in the Bay of Biscay. The purpose of this study was not to develop new statistical methods for estimating egg mortality rates but to estimating the percentage of anchovy egg mortality that is due to cannibalism and the percentage that is due to predation by small pelagic species, providing a simple solution for calculating egg consumption by all potential predator species (including cannibalism) sharing the same niche and allow comparisons with estimates in other ecosystems. To assess the validity of our estimates, results from calculations utilizing both the proposed methodology and the equations used in the previous literature are compared in a sensitivity analysis. This is the first approach to understand the role of the intraguild predation on regulation of anchovy population in the Bay of Biscay.


Materials and methods Both anchovy eggs and adults were sampled in the whole anchovy spawning area of the Bay of Biscay during two DEPM-based anchovy spawning stock biomass estimation surveys, BIOMAN2008 (6 May–26 May) and BIOMAN2009 (5 May–25 May). Plankton sampling was carried out on board the R/V Investigador. The anchovy egg sampling followed a systematic central sampling scheme with a random origin and sampling extension depending on the egg abundance found (Uriarte et al. 1999). Vertical hauls of 150-µm PAIROVET nets (Smith et al. 1985; Wiebe and Benfield 2003) were used to collect plankton samples (nBIOMAN’08 = 544; nBIOMAN’09 = 409). The net was lowered to a maximum depth of 100 or 5 m above the bottom in shallower areas. Samples were preserved immediately after collection in 4 % borax-buffered formaldehyde solution (Harris et al. 2000). After a minimum of 6 h of fixing, anchovy eggs, sardine eggs and “other eggs” were identified, sorted and counted on board. Later in the laboratory, a portion of the samples was checked under a stereomicroscope (model NIKON SMZ645) to assess the quality of the sorting made at sea. Simultaneously to the plankton sampling, adult samples of European anchovy (E. encrasicolus), sardine (S. pilchardus), Atlantic horse mackerel (T. trachurus), Mediterranean horse mackerel (T. mediterraneus), Atlantic mackerel (S. scombrus), Atlantic Chub mackerel (S. colias), bogue (Boops boops) and sprat (Sprattus sprattus) were obtained with pelagic trawls on board the R/V Emma Bardán. Once the fishing hauls had been collected (nBIOMAN’08 = 10; nBIOMAN’09 = 11), the fish were measured and weighed and then frozen for preservation. Collection of fish was made during trawls in which anchovy and at least one of the other predator species were caught. Fish samples were collected during both day and night in the cases of all predator species, covering as wide a size range as possible during the fish collection. A constant number of 15 fish stomachs per station were analysed whenever the catch size permitted (sampling of S. colias was sparse). In the laboratory, the fish were thawed and their stomachs extracted, weighed and stored in 4 % borax-buffered formaldehyde solution for later examination. The fish stomachs were excised with tweezers and a scalpel, and their contents were extracted into the trophometer, a tool used for bulk estimations, which consists of a set of graduated half cylinders of different volumes, in which the stomach contents are placed to measure the volume, called the “repletion index” (Olaso 1990; Bachiller 2012). To exclude a fish size effect, the repletion index was weighted by the total weight of fish in later analyses. The stomach contents were examined under a stereomicroscope, and anchovy eggs were identified and counted. Empty stomachs were omitted from the analysis.

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As a first exploratory analysis, nonparametric tests (Shapiro–Wilk test, P 100 %, Table 6). All the estimates were lower when the total biomass of the predator fish was estimated by considering only the

spawning area of the anchovy (DEPM biomass); in the case of the impact of cannibalism, values decreased by 51–52 and 34–36 % in 2008 and 2009, respectively. For the egg mortality due to sardine predation, estimations decreased by 72–75 % when the assumed total sardine biomass was limited to the spawning area of the anchovy (Table 6). In any case, it seems clear that sardine predation resulted in a relatively higher impact on anchovy egg mortality in both years (Table 6), showing higher results than other predator species, not only in comparison with anchovy (Table 6) but also in comparison with the other sampled small pelagic species (Table 5).

Table 5 Parameters and calculations for estimating daily predator egg consumption and percentage of total anchovy egg mortality due to egg cannibalism and predation by other predator fish species in (a) BIOMAN 2008 and (b) BIOMAN 2009 2008 Gt = 1.78E+12 Zt = 0.62 EE′

n

C′ (t′ = 12 h)

Ct (t′ = 12 h)

Bp

% Zc

% Pc (CV)

(a) E. encrasicolus

94

43

218

3.27E+07–4.20E+07

7.13E+09–9.16E+09

0.46

0.74 (0.18)

S. pilchardus

90

337

853

3.63E+08–4.83E+08

3.10E+11–4.12E+11

20.27

32.69 (0.20)

T. trachurus

90

0

0

2.34E+07–8.11E+07

0

0.00

0.00

T. mediterraneus

–

–

–

1.10E+05–1.72E+05

–

–

–

S. scombrus

63

23

50

2.64E+08–1.16E+09

1.33E+10–5.85E+10

2.01

3.24 (0.89)

S. colias

7

12

27

8.07E+05–1.40E+06

2.14E+07–3.72E+07

1.64E−03

1.01E−03 (0.38)

B. boops

11

2

5

–

–

–

–

S. sprattus

10

321

127

7.30E+06–1.21E+07

9.22E+08–1.53E+09

0.07

0.11 (0.35)

2009 Gt = 1.70E+12 Zt = 0.57 n

EE′

C′ (t′ = 12 h)

Bp

Ct (t′ = 12 h)

% Zc

% Pc (CV)

(b) E. encrasicolus

120

26

131

3.10E+07–3.88E+07

4.07E+09–5.10E+09

0.27

0.47 (0.16)

S. pilchardus

110

47

119

4.33E+08–5.27E+08

5.16E+10–6.28E+10

3.36

5.91 (0.14)

T. trachurus

141

0

0

5.15E+07–6.17E+07

0

0.00

0.00

T. mediterraneus

71

0

0

–

–

–

–

S. scombrus

90

2

4

–

–

–

–

S. colias

–

0

0

–

–

–

–

B. boops

44

8

26

–

–

–

–

S. sprattus

40

15

6

1.00E+08–1.25E+08

6.06E+08–7.57E+08

0.04

0.07 (0.16)

Gt is the total daily egg production (data source: BIOMAN DEPM surveys by AZTI, ICES 2008, 2009), and Bp is the total biomass (kg) of fish predators (data source: PELGAS’0408 & 0409 acoustic survey estimates by IFREMER, ICES 2008, 2009). Calculations for the following parameters are explained in the main text: Zt (proportion of egg production lost due to all causes of mortality), EE′ (average number of anchovy eggs eaten per kg of predator, adjusted to the total weight of the fish caught and the trawling time at each station), C′ (average number of anchovy eggs eaten daily per kg of predator), Ct (total number of anchovy eggs eaten daily), % Zc (proportion of anchovy egg production consumed by cannibalism or other fish predation) and % Pc (proportion of anchovy egg mortality caused by cannibalism or other fish predation). CV is the coefficient of variation of the mean anchovy egg mortality rate (Pc) depending on the assumed total predator biomass (Bp)

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Table 6 Pc (%) estimations for anchovy and sardine predation in 2008 and 2009, depending on the equation used for EE′ calculation (Table 1), duration of feeding (t = 12 vs. 24 h), total predator biomass Equation (1)

This study

t

12 h

Hunter and Kimbrell (1980) 24 h

12 h

% change (Eq)

24 h

Biomass assumed E. encrasicolus 2008 0.74 Bp 0.36 Bp′ % change (B) (−51.35) 2009 0.47 Bp

1.48

0.49

0.99

(+51.02)

0.71

0.24

0.48

(+50.00)

(−52.03) (−51.02) (−51.52) 0.95

0.41

0.81

(+14.63)

0.31 0.61 0.26 0.52 (+19.23) Bp′ % change (B) (−34.04) (−35.79) (−36.59) (−35.80) S. pilchardus 2008 32.69 Bp 8.97 Bp′ % change (B) (−72.56) 2009 5.91 Bp Bp′

1.49

65.39

214.01

428.02

(−84.73)

17.93

58.69

117.38

(−84.72)

(−72.58) (−72.58) (−72.58) 11.80

8.47

16.94

(−30.22)

2.97

2.14

4.27

(−30.37)

% change (B) (−74.79) (−74.83) (−74.73) (−74.79) Values in bold are those corresponding to Eq. (1) and assumptions used the present study (i.e. from Table 5). % change (Eq) is the percentage change of values obtained with Eq. (1), considering the equation from Hunter and Kimbrell (1980) as reference; % change (B) is the percentage change between Pc depending on the total biomass of predators assumed, i.e. total area of distribution (acoustic estimations, as reference) versus spawning area of the anchovy Bp total biomass corresponding to the whole distribution area, Bp′ predator biomass corresponding to the spawning area of the anchovy, source: BIOMAN DEPM, see text for more details

Discussion Potential predator distribution in relation to anchovy egg distribution The highest anchovy egg concentrations are observed in the areas under the influence of the major river plumes (Gironde and Adour) and near Cap Breton, which are the main spawning areas of the anchovy (e.g. Motos et al. 1996; this study). Accordingly, the catches of adult fish mainly taken in these areas allow us to determine the impact of predation by different predators on anchovy egg mortality. The composition of fish species in our hauls fits well to the species distribution observed with acoustic methods in the same area and season (ICES 2008, 2009). Moreover, the distribution of adult anchovy matches typical

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anchovy spawning areas (Motos et al. 1996), which are associated with rich waters under the influence of major river plumes (Gironde and Adour) or are located close to other productive areas like the shelf break, in particular Cap Breton. Sardines share the same niche as anchovies in spring (Planque et al. 2007; ICES 2011a) and are especially abundant close to the shore over the Cantabrian and French continental shelves (especially in the latter in 2009) (ICES 2008, 2009). Furthermore, they seem to be close competitors for the same food resource, especially in terms of prey size (Bachiller and Irigoien 2013). The same could be said about sprat (Bachiller and Irigoien 2013), although this species is closely related to the Gironde River plume (Massé 1996; ICES 2008). Atlantic and Atlantic Chub mackerel show a wide distribution in the Bay of Biscay, limited in part by the hydrographical conditions (Villamor et al. 2011) and by seasonal fluctuations related to their life cycle (Conway et al. 1999). Atlantic and Mediterranean horse mackerel show seasonal and inter-annual variations (ICES 2011b) and are also widely distributed along the Bay of Biscay. In addition, few samples of bogue were taken around the Cantabrian area in 2008 and 2009. Although there is no literature about the distribution of this species in the Bay of Biscay, results suggest a distribution close to the Cantabrian area, sharing the same niche with the horse mackerel of the southern part of the Bay of Biscay. This is also in accordance with observations during the PELACUS 2008 and 2009 surveys, carried out by the IEO (ICES 2008, 2009). Anchovy egg mortality due to predation Anchovy egg ingestion varied depending on the sampling year and potential predator species. According to the survey effect on the amount of eggs found in stomachs, results showed that, despite a high variability between stations (and individuals), those stations in which higher anchovy egg ingestion was detected fit well with the main spawning areas of the anchovy (detailed comments are made for each species throughout this section). The repletion index was not a good indicator of the amount of anchovy eggs ingested, since many fish had full stomachs without any egg in their contents. However, considering only the fish that ingested anchovy eggs, those with high number of eggs in their gut contents also exhibited relatively fuller stomachs (i.e. higher repletion indices), suggesting a positive relationship between the feeding activity and the number of eggs ingested. Hence, in the Bay of Biscay, anchovy eggs available during the spawning period could be an interesting feeding resource for different small pelagic species including the anchovy itself (e.g. Santander et al. 1983; Pájaro 1993; Pájaro et al. 2007; Irigoien and De Roos


2011). On the other hand, differences between predator species could be due to their feeding behaviour and/or diet preference. However, it is still not clear if anchovy eggs are ingested through selective feeding or continuous filter feeding behaviour (see comments about the duration of feeding in the “Introduction” section), and prey preference could not be determined here. Nevertheless, all fish sampled were adults, and therefore, the whole fish size range was considered as potential predators for such small items like anchovy eggs (Bachiller 2012; Bachiller and Irigoien 2013). Whatever the methodology used for the consumption estimation, results show that the sardine species is the main consumer of anchovy eggs and one of the major causes of anchovy egg mortality, which is in accordance with the findings presented by Alheit (1987). For the Bay of Biscay, assuming a duration of feeding of 12 h and the total area of distribution, the estimated anchovy egg mortality caused by sardine predation is somewhere between 28 and 37 % (mean Pc = 33 %) in 2008, and between 5 and 6 % in 2009. This estimation for 2008 is close to the 56 % found in South Africa assuming a duration of feeding of 24 h (Valdés Szeinfeld 1991), being 65 % if the same feeding period (i.e. continuous filter feeding activity during the night hours) is assumed (Table 6). If the total sardine biomass was considered only in the spawning area of the anchovy (sardine biomass from the stations with presence of anchovy eggs, DEPM surveys), egg mortality caused by sardine predation could reach 9 % (e.g. in 2008, Table 6). Regardless of the methodology used for the estimations, Bay of Biscay sardines exhibit the maximum egg predation values in the waters surrounding Cap Breton and the French continental shelf, especially the area under the influence of the Adour and Gironde River plumes, where the concentration of anchovy eggs is relatively high in accordance with the main anchovy spawning areas (Motos et al. 1996). Cannibalism by anchovy occurs in the entire spawning area, but the total egg mortality caused by this activity (t′ = 12 h) does not exceed 1 % (whatever predator distribution area is used), which is also in agreement with the lowest estimates observed by Valdés Szeinfeld (1991) for the South African anchovy and Pájaro et al. (2007) for the Argentine anchovy (t′ = 24 h). In the case of the latter, a decrease in egg cannibalism was observed as the copepod density increased (Pájaro et al. 2007) and that could also happen in the Bay of Biscay due to the high zooplankton density in the anchovy spawning area (e.g. Plounevez and Champalbert 1999; Bachiller et al. 2013). The impact of other predators is lower, either due to no ingestion of eggs (e.g. horse mackerel), a lower overlap between the distribution and the main spawning areas (e.g. mackerel) or reduced distribution (e.g. sprat). However, at least in 2008, somewhere between 2 and 5 % of

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egg mortality could be attributed to predation by other fish, which, together with sardine, indicates that, considering the coefficient of variation for total predator biomass (i.e. acoustic estimations), 31–43 % of anchovy egg mortality can be attributed to predation by small pelagic fish. The overall impact estimated for 2009 may reach somewhere between 6 and 8 %. The consumption estimations varied (Table 6) depending on (1) the feeding period assumed for the anchovy egg consumption estimation (% change in Pc = 50 from 12 to 24 h), (2) the adjustment made for the total egg consumption per kg of fish and day, i.e. EE in Eq. (1) (% change in Pc = 20–80 % depending on the species and sample year) and (3) the biomass of predators assumed (% change in Pc = 34–75 %). According to our analysis, it seems clear that the mean egg consumption estimation (EE) adjustment is one of the most critical factors for such estimations. The impact of sardine predation on anchovy egg mortality shows high values in accordance with estimations obtained in other systems, even in those where the sardine biomass is by far lower than that of the anchovy, e.g. Argentina (Pájaro et al. 2007). In the Bay of Biscay, where the sardine biomass is much higher than that of the anchovy (e.g. ICES 2011b) and with few sardine individuals showing the maximum values of eggs in gut contents (i.e. more than 1000 eggs in a single fish obtained in our limited sampling set), the lack of adjustment with cpue (i.e. following the method by Hunter and Kimbrell 1980) results in a clear distortion of total egg consumption estimates and therefore in estimated egg mortality rates due to predation (Pc > 100 %, Table 6), especially if differences between total predator biomasses are as high as those observed between anchovy and sardine in the Bay of Biscay. Regarding the total predator biomass assumed, the acoustic estimates clearly overestimate the potential predator distribution since they consider also areas with relatively low or even no anchovy eggs (e.g. ICES 2011a, b), but are instead useful for relative comparisons between the species and applied methodologies. Thus, it seems clear that assuming a predator biomass limited to the anchovy egg distribution area, as presented as a case for anchovy and sardine, would be more appropriate. However, it should be noted that the total biomass estimates for anchovy and sardine in the spawning area of the anchovy are still biased by the trawling methodology, since the DEPM surveys aim to catch anchovies during the peak spawning (i.e. at dusk and night time, close to the surface) (ICES 2008, 2009) and therefore could underestimate the anchovy and sardine biomasses that could potentially be feeding on anchovy eggs during daytime. In fact, although a reduction in the estimated Pc rates is expected when considering a reduced area of distribution for predators (i.e. the spawning area of the anchovy), the percentage change was reasonably higher for the estimated impact by sardine

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predation (Table 6), which is in accordance with the suggested underestimation problem for sardine biomass if estimated from the DEPM survey data. The limited sampling effort could also affect the representative perspective of the potential variations in anchovy egg predation that can occur over a broad sampling region. Further, estimations considering the predator biomass from the DEPM surveys are not available for other potential predator species (e.g. mackerel, horse mackerel, bogue and sprat), and the same could be said for the acoustic information in the case of bogue and sprat biomass and distribution. Because they are not commercial species, there is little information on their populations. Hence, it might be interesting to make predator biomass catch estimates (i.e. biomass estimates for each predator species at each station or corresponding area) in order to obtain more accurate potential predator biomass estimates. Moreover, this would allow further comparisons of the egg mortality caused by predation to be made, e.g. day versus night comparisons or mortality caused by predation of different species in different areas. Nevertheless, our results show that fluctuations in anchovy egg mortality and therefore in the survival index of early life stages of the anchovy in the Bay of Biscay can be at least partially due to intraguild predation (including cannibalism but also other species like Atlantic horse mackerel or sprat) and especially to high sardine predation on anchovy eggs. However, assumptions should be considered to obtain accurate estimates of egg mortality and previously to manage the predators of a spawner to include mortality targets for the early life population. Obviously, the main source of inter-annual variability in the mortality rate due to predation is the variability in predator abundance and its overlap with the anchovy spawning area. That said, fluctuations in the main source of predation mortality of anchovy eggs still remain partially unexplained. For example, in case of sardine, there is not a change in the total biomass from year to year, but it is in the predation impact; on the other hand, there is an equally dramatic inter-annual change in egg consumption by sprat, but this seems to be compensated by an opposite dramatic change in sprat abundance (Table 5). This could suggest two different points: (1) temporal fluctuations on different predator biomass have to be deeply considered in this kind of mortality estimates since very large inter-annual fluctuations affect the system and that the results obtained from Eq. (2) are sensitive to them; (2) other variables could also affect the impact by predation on the mortality of eggs (e.g. the diet preference, predation success, consumption-energy requirements, etc.). Unfortunately, these two aspects could not be answered with the available data in this study. Up to now, most surveys in the Bay of Biscay have focused in the estimation of the biomass of a single species (surveys of anchovy and of mackerel, e.g. ICES 2009,

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2011b). In this sense, further research should consider predator sampling centred within the spawning area of the anchovy in order to obtain more accurate potential predator biomass estimates. Otherwise, the obtained consumption values could be overestimated since those predators feeding out of the spawning area would also be considered as potential predators. In addition, egg consumption estimates should be made for each of the stations, adjusting the number of eggs per kg of fish according to the cpue; this seems to be the best option to take into account the high individual variability observed between the stomach contents. The duration of feeding, diet overlap, diet preference or required energy intake for survival (i.e. consumption requirement) would be other variables that could make this kind of estimates more accurate. On the other hand, higher spatial resolution would allow making consumption estimates more representative of the area, detecting also the potential variations that can occur over the region. Longer time series of anchovy egg counts in potential predator gut contents would also allow inter-annual variations in both anchovy egg consumption estimates and predator-induced egg mortality rate estimates to be checked. Understanding different factors affecting recruitment is still a difficult task that requires making many assumptions (and that has been also observed in previous studies) so that with the little available information in this field, we cannot expect improvements in recruitment estimations. However, similar analyses as the one presented here could help us to understand why the high biomass of a specific predator could play an important role as a regulation mechanism of another species’ population (Smith and Reay 1991; Irigoien and De Roos 2011) and would also be helpful to explain (at least in part) the variability of the mortality of eggs considered in DEPM estimations. In fact, the natural mortality rates estimated for 2008 and 2009 were 0.57 and 0.62, respectively (ICES 2008, 2009), and these could be higher if predation impact were considered. Moreover, DEPM surveys are developing new methods to estimate the spatial variability of anchovy egg mortality rates (Stratoudakis et al. 2006), and this could allow changes to be reflected in the predation and/or cannibalism of eggs. This could be of special interest to understand processes affecting the recruitment of the anchovy, moreover, taking into account that the main spawning area corresponds to the continental shelf, where most of this predation seems to occur not only by sardine (which seems to be the most relevant) but also by other potential predators like sprat or anchovy itself. Nevertheless, rather than basing conclusions in concrete mortality rate numbers obtained with different methods, the results from the various equations clearly reflect that, at least in the Bay of Biscay, the predation by small pelagic fish (especially intraguild predation by sardine and cannibalism) is an important source for anchovy egg mortality. Limitations


when using different equations also show how important is to have multispecies surveys with spatial distribution and biomass estimates for the different components of the pelagic ecosystem (e.g. Gislason 1999; Huse et al. 2012). In this sense, an ecosystem approach to fisheries management needs to consider that the highest mortalities occur at the earliest stages, but also that the predators of these stages are not the same than those of the adults. In any case, accurate estimates not only of egg but also of larval mortality due to intraguild predation can be of special interest in understanding shifts in the equilibrium between species (Irigoien and De Roos 2011), as in case of anchovy and sardine of the Bay of Biscay. Acknowledgments We are grateful to the captains and crew of the research vessel R/V Emma Bardán, as well as to the onboard scientists and analysts for their support during the sampling and laboratory work. Very special thanks are due to Marcelo Pájaro (INIDEP) for his help with the parameter calculations. We would also like to thank the Editor and the four anonymous reviewers who provided insightful comments that greatly improved the manuscript. This work was funded by the Ecoanchoa project (FEP Project, Department of Agriculture, Fisheries and Food of the Basque Country Government) and the EU FP7 FACTS (Forage Fish Interactions) project, Grant Agreement No. 244966. Eneko Bachiller was supported by a doctoral fellowship (2007–2011) from the Iñaki Goenaga Zentru Teknologikoen Fundazioa (IG-ZTF) and by a postdoctoral fellowship (2014–2016) from the Department of Education, Language policy and Culture of the Basque Country Government (EJ-GV). This is Contribution No. 712 from AZTI-Tecnalia (Marine Research Division).

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