Monitoring small fish populations in streams: A comparison of four passive methods M. Clavero a,b,∗ , F. Blanco-Garrido b , J. Prenda b Institut d’Ecologia Aquàtica, Universitat de Girona, Facultat de Ciències, Campus Montilivi, 17071 Girona, Spain b Departamento de Biologı́a Ambiental y Salud Pública, Universidad de Huelva, Campus Universitario de El Carmen, Avda. Andalucı́a s/n, 21071 Huelva, Spain a Abstract We analysed the relative efficiencies and size-selectivities of four different passive capture methods in a small coastal stream. We used plastic minnow traps (PM), metal minnow traps (MM) and two types of fyke nets differing in mesh size (F1, small meshed; F2, large meshed) to capture over 12,000 fish belonging to 11 species. Over 97% of captured fish were Andalusian toothcarp (Aphanius baeticus), Iberian loach (Cobitis paludica) and sand smelt (Atherina boyeri). F1 was the most efficient trap type in capturing the three most abundant species. Catches by PM and F2 differed in taxonomic composition, the former being characterised by toothcarp and loach dominance and the latter by the catch of eel (Anguilla anguilla) and grey mullets (Fam. Mugilidae). There were large differences in the size of fish captured in each trap type, with fish size following the pattern F2 > MM > F1 > PM. Small juveniles of the three dominant species were captured only in PM, thus enabling us to follow their seasonal size variation. However, PM traps were inefficient for sand smelt sampling and failed to catch large individuals of this species. This schooling and mainly pelagic species was more accurately monitored through the use of F1. Our results suggest that a combination of PM and F1 traps could improve the efficacy of small fish sampling in streams. Keywords: Survey methods; Passive techniques; Efficiency; Selectivity; Stream fish 1. Introduction Entrapment devices are among the most ancient fish collecting techniques used by humans (Hubert, 1996). They have been used to assess issues such as fish density and habitat use (e.g. Gryska et al., 1998; Clavero et al., 2005). Captures in fish traps rely on fish movement, and traps must be equipped with some type of structure that deters fish from leaving the trap once they have entered (Craig, 1980). If traps are unbaited, captures should be positively related to each trap’s interception area (the area directing to the funnel) and inversely related to the escape rate (depending on factors such as mesh size) (Blaustein, 1989). ∗ Corresponding author. Tel.: +34 972 41 84 67; fax: +34 972 41 81 50. E-mail addresses: miguel.clavero@udg.es (M. Clavero), jprenda@uhu.es (J. Prenda). Various authors have criticised the use of traps to study fish populations. They have been reported to have low efficiency (Jackson and Harvey, 1997), to be size-selective (Hubert, 1996) and to be influenced by the presence of fish already trapped (He and Lodge, 1990). However, in some conditions traps might be the only available method to make effective and comparable surveys of fish populations. This could be the case for fish species occupying a broad habitat spectrum, since each fishing technique has different limitations. For example beach seining would be limited by aquatic habitat structure (Bunt et al., 1998), direct observations by water depth, velocity or turbidity (Heggenes et al., 1990) and electrofishing by water salinity and depth, apart from being inefficient on small fish or species lacking swim bladder (Reynolds, 1996). Thus, if passive traps are to be used, it would be necessary to assess the efficiency and size selectivity of different trap designs. In the present study we compare the captures produced by four different passive devices (two minnow traps and two fyke nets) in a small coastal stream in terms of diversity, efficiency and size selectivity. The three most abundant species in the study area, Andalusian toothcarp (Aphanius baeticus Doadrio, Carmona & Fernández-Delgado 2002), henceforth toothcarp, Iberian loach (Cobitis paludica de Buen 1930), henceforth loach, and sand smelt (Atherina boyeri Risso 1810), have special features that make them difficult to survey with techniques other than passive methods. Toothcarp is a euryhaline species that inhabits mainly saline streams, but also freshwater streams and lagoons (Prenda et al., 2003). Sand smelt’s main habitats are estuarine areas, but the species can also be found in lenthic and lotic freshwater systems (Rosecchi and Crivelli, 1992; Leonardos, 2001). Due to the wide variety of habitats occupied both by toothcarp and sand smelt, repeatable surveys of their populations can only be performed through the use of passive methods. The loach is a bottom dwelling stream species lacking a swimbladder (Perdices and Doadrio, 1997), a characteristic that is usually associated with difficult sampling through active fishing methodologies (Bunt et al., 1998; Reyjol et al., 2005). Toothcarps are small, rarely surpassing 50 mm (TL), and short-lived, with only around 10% of winter populations belonging to age classes 1+ or 2+. Reproduction occurs from spring to autumn. Individuals born during spring and early summer take part in late-summer and autumn reproduction events (Fernández-Delgado et al., 1988). Sand smelt reach around 110 mm TL and up to age 4+ (Leonardos, 2001). Breeding has been reported to occur between March and July (Rosecchi and Crivelli, 1992). Maximum loach sizes reported in the literature range from 90 to 100 mm, reaching 5 years of age (Soriguer et al., 2000; Oliva-Paterna et al., 2002). Reproduction events occur from March to July (Oliva-Paterna et al., 2002). These three species are considered endangered in Spain according to IUCN criteria (Doadrio, 2001), especially toothcarp, which is considered critically endangered (CR) due to a very restricted range with only eight extant populations (Doadrio et al., 2002). It would be therefore necessary to establish repeatable sampling procedures that would allow appropriate comparisons of density, population structure and habitat use among different toothcarp, loach or sand smelt populations. 2. Material and methods 2.1. Study area This study was conducted in the La Vega River (S. Spain), a 13 km long coastal stream with a drainage area of around 20 km2 . Traps were set in a 600 m freshwater stretch located just upstream of the tidal section of the river. This has a highly variable regime following a typical Mediterranean cycle, with only a few isolated pools retaining water during summers. Therefore, traps were always set in pools, in order to maintain as many as possible constant sampling points. 2.2. Trap types and fish sampling We used four different types of traps in this study, two kinds of minnow traps (PM and MM) and two fyke nets (F1 and F2) with different mesh sizes (Table 1). PM traps were made with 2 L soda plastic bottles (Fouilland and Fossati, 1996). The upper piece of each bottle was cut and inverted, acting as a funnel. PM traps were set in the bottom of the stream fixed with a metal stake (6.5 mm diameter). MM traps were made of a galvanized metal mesh (6 mm) with steel ringframes and were composed of two symmetrical pieces, each one with a funnel at its end. These traps were directly set in the stream bottom. F1 nets consisted of a semicircular entrance ring followed by three smaller circular rings surrounded by a net (3.5 mm mesh) and had two consecutive funnels. F2 nets were similar in shape, but had five circular rings, larger meshed net (7 mm) and three funnels. Each fyke net had a single net wing directed towards the entrance funnel, which was always placed in the downstream direction. Two metal stakes (8 mm diameter) were used to fix each fyke net to the stream bottom. Thirteen surveys were performed in the study area between July 2002 and August 2004 (Table 2). MM traps were used only in the last six surveys. PM and MM traps were used both during daytime and at night, while fyke nets were set only at night. Fish trapping was performed in one day and one night in each survey. The mean trapping time was 4.5 h (±1.6 h, S.D.) for daytime traps and 15.0 h (±2.1 h, S.D.) for night time ones (Table 2). Night time traps catches could also include some fish caught in traps during early morning. However, considering all captured fishes in these traps as “night captures” is a conservative assumption, since possi- Table 1 Main characteristics of the four trap types employed in River La Vega PM MM F1 F2 Mesh size (mm) Funnel diameter (mm) Interception area (cm2 ) Length (cm) Height (cm) Wing length (cm) – 6.0 3.5 7.0 21.5 22.0 120.0 170.0 72 567* 1050 1946 22.5 42 98 192 9.6 22 30 43 – – 95 110 PM, plastic minnow trap; MM, metal minnow trap; F1 and F2, fyke nets. The interception area is the maximum area within the water column which leads to the funnel. MM trap value is marked (*) because it corresponds to the sum of the two intersection areas (see method for trap description). × × × × × × 7.2 ± 0.9 14.2 ± 2.1 2.5 ± 0.4 13.2 ± 0.5 Au Jl × × 4.2 ± 0.2 15.2 ± 1.6 × × 4.5 ± 0.7 14.0 ± 3.0 × × 6.0 ± 0.6 16.3 ± 0.6 × × 4.7 ± 0.9 16.0 ± 2.5 × × 2.5 ± 0.2 17.0 ± 1.3 × × 3.7 ± 0.9 11.7 ± 0.9 × × 4.4 ± 0.6 17.2 ± 0.2 Jn × × × × 5.2 ± 0.2 13.8 ± 1.2 × × × × 5.9 ± 0.5 13.5 ± 0.8 My Ap × × × × 6.5 ± 0.8 13.9 ± 1.3 × × × × 3.0 ± 0.0 16.7 ± 1.0 Ja Sp × × × × Jl My Ja × × × Oc Au Jl PM MM F1 F2 Day Night 2004 2003 2002 Table 2 Trap deployment and mean soak times (±S.D.) for day and night sets during the study period ble morning captures would tend to homogenise daytime and night results. Each captured fish was identified, measured to the nearest millimetre and released. Traps were always set unbaited. 2.3. Data analysis Fish captures were expressed as catch per trap (CPT). It is possible that catches in traps reach some type of saturation, with entry rates decreasing with increasing trapping time. Soak time (in h) was therefore introduced as covariate when analysing CPT values, and maintained in the models whether it did or did not have a significant influence on CPT. For each trap we calculated the CPT of every fish species, the total CPT of fish and the number of fish species caught. Prior to statistical analyses CPT data were logarithmically transformed [log10 (X + 1)], due to the high proportion of zero values and the heavily right-skewed distribution of the data. To analyse the main patterns in the taxonomic composition of captures between trap types we pooled the capture results of each trap type by surveys, also separating CPT data from daytime and night trapping in the cases of PM and MM traps. This generated a matrix of 59 rows and 6 columns. This matrix was submitted to a principal components analysis (PCA). Only principal components with eigenvalues larger than 1 were analysed (latent root criterion; McGarigal et al., 2000) and they were interpreted through correlation analysis and one-way ANOVA. Data on grey mullet catches (Fam. Mugillidae, at least three species) were pooled and species that had been recorded in less than five surveys–trap types were excluded from the PCA. We studied differences in trap efficiency through a GLM design, using CPT of the most abundant species as dependent variable, soak time as covariate and trap type, time (day–night) and survey as fixed factors. In all cases we ran full models, including all interactions among fixed factors. The effect of trap type on average size of captured fish was assessed through one-way ANOVA. Factorial ANOVAs, with trap type and survey as fixed factors, were also performed to include the effect of seasonal variation of mean fish size. 3. Results 3.1. Taxonomic selectivity and trap efficiency During the study period we set 1080 PM traps, 187 MM traps, 60 F1 nets and 54 F2 nets. We captured 12,346 fish belonging to at least 11 species (Table 3). Toothcarp, loach and sand smelt comprised over 97% of the captures. Relatively low numbers of Iberian chub (Squalius pyrenaicus Gü nther 1868), eel (Anguilla anguilla L. 1758) and grey mullets (flathead Mugil cephalus L. 1758, thick-lipped Chelon labrosus Risso 1826 and Liza spp.) were also caught. Occasionally encountered species included common goby (Pomatoschistus microps Krøyer 1838), European sea bass Table 3 Number of individuals of the different fish species captured in the four trap types during the study period PM Andalusian toothcarp Iberian loach Sand smelt Iberian chub Eel Flathead grey mullet Thick-lipped grey mullet Mullets Black-stripped pipefish Common goby European sea bass Total Aphanius baeticus Cobitis paludica Atherina boyeri Squalius pyrenaicus Anguilla anguilla Mugil cephalus Chelon labrosus Liza spp. Syngnathus abaster Pomatoschistus microps Dicentrarchus labrax MM F1 F2 Total 4025 1833 904 52 12 3 – 11 10 12 – 334 188 447 65 8 – – 38 – – – 379 400 3419 12 29 6 – 20 – – – 9 6 61 10 28 7 10 7 – – 1 4747 2427 4831 139 77 16 10 76 10 12 1 6862 1080 4265 139 12346 (Dicentrarchus labrax L. 1758) and black-stripped pipefish (Syngnathus abaster Risso 1810). The PCA generated two gradients in the composition of captures along the study period (Fig. 1). PC1 represented a gradient running from low to high total CPT (r = 0.96; P < 0.001) and was positively related with the CPT of all fish species. F1 nets scored higher along PC1 that any other technique (F3,55 = 21.4; P < 0.001), denoting a higher general efficiency of these nets. PC2 was not related to total CPT, but to the taxonomic composition of captures. PM traps had captures dominated by toothcarp and loach and occupied positive positions along PC2, while F2 nets were placed towards the negative extreme with higher CPTs of eel and grey mullets (F3,55 = 20.8; P < 0.001). The number of fish species caught was negatively correlated with PC1 (r = 0.39; P < 0.01) and PC2 (r = −0.37; P < 0.01). However, this variable did not show significant differences among trap types when data had been pooled by surveys (F3,55 = 1.3; P = 0.28). Catches of toothcarp, loaches and sand smelt showed large variations in the different surveys performed during the study period (Table 4). Differences between night and day catches were significant only in the case of loach. Trap type had a clear influence on CPT of the three species, but there were also significant effects of the interaction between trap type and survey. F1 nets were the most efficient traps in capturing the three species (Fig. 2). However, during some surveys, particularly those performed in July, toothcarp captures were similar in F1 and PM traps. In summer surveys, loach captures tended to be higher in PM traps than in MM or F2, but CPT values from the three methods were similar in other seasons. The higher efficiency of F1 in capturing loach and sand smelt was consistent in all surveys performed during the study period. 3.2. Size selectivity There were highly significant differences in the size of fish captured using the four trap types (F3,12342 = 1684.3; P < 0.01). The general trend in captured fish size was PM < F1 < MM < F2 (Table 5). This trend was also evident when the three dominant species were analysed independently (Fig. 3), though the variation of captured fish size among trap types had special features for each of the species. The maximum sizes of both toothcarp and loach were simTable 4 Results of the GLMs using CPT of toothcarp, loach and sand smelt as dependent variables, soak time (h) as covariate, and trap type (M), time (T, day–night) and survey (S) as fixed factors d.f. Soak time M T S M×T M×S S×T M×T×S Fig. 1. Scores of each trap type in the space defined by the first two components of the PCA applied to a matrix of log-transformed catch per trap (CPT) of six fish species. For PM and MM solid circles denote night traps and empty circles daytime ones. PC1—eigenvalue = 2.4; 39.8% expl. var.; PC2—eigenvalue = 1.4; 23.3% expl. var. Error * ** *** 1 3 1 12 1 27 12 4 1253 Significant at P < 0.05. Significant at P < 0.01. Significant at P < 0.001. F toothcarp F loach F sand smelt 0.8 14.4*** 0.4 5.0*** 5.3* 1.8** 0.7 1.3 8.1** 29.4*** 16.6*** 4.3*** 1.4 1.9** 1.6 0.4 0.1 277.5*** 0.1 15.8*** 0.5 9.6*** 0.8 0.5 Fig. 2. Marginal means (±S.E.) of the CPT values of toothcarp, loach and sand smelt, as estimated by the GLM. Graphics on the left show CPT values for the different trap types in all performed surveys (PM traps—solid circles, solid line; MM traps—solid triangles, solid line; F1 nets—empty circles, dotted line; F2 nets—empty triangles, dotted line). Graphics on the right show CPT values estimated for the four different trap types analysed. ilar for the four trap types, suggesting that none of the devices imposes upper limit restrictions to the capture of these species. That was not the case of sand smelt, whose maximum size in PM traps was much smaller than that in other trap types. On the other hand, PM traps captured the small individuals of the three species that could not be taken using any other trap type (Table 3). Most loaches captured in MM traps and F1 nets fell within a narrow interval of sizes, especially in MM traps, since over 55% of loaches captured in these traps measured between 55 and 62 mm (Fig. 3). During the study period there were clear seasonal differences in the mean fish size of the populations of the three species under analysis (F > 11.0; P < 0.01 in the three cases). “Trap type” had a strong influence in the mean size of fish Table 5 Mean, minimum and maximum sizes (in mm) of the different species, or group of species, captured using the four trap types PM Toothcarp Loach Sand smelt Other fish (except eel) Eel MM F1 F2 Mean Min. Max. Mean Min. Max. Mean Min. Max. Mean Min. Max. 24.5 38.6 33.1 49.8 95.6 10 14 12 14 67 56 95 70 130 280 40.8 64.7 59.6 71.0 283.7 20 50 42 40 200 58 96 92 211 325 32.1 54.0 41.2 51.3 261.5 16 31 18 23 110 54 98 112 193 450 44.5 82.6 74.5 112.8 340.3 39 71 51 60 240 50 96 96 220 570 Fig. 3. Size frequency distribution of captured toothcarp, loach and sand smelt in each trap type. Intervals are 1 mm in the case of toothcarp and 2 mm for loach and sand smelt. caught once “survey” and the interaction “survey × trap type” had been included in the model (toothcarp, F3,4712 = 135.2; loach, F3,2383 = 197.6; sand smelt, F3,4792 = 121.4; P < 0.01 in all cases). Moreover, catches in the four trap types showed different patterns when describing the seasonal changes in the size structure of fish populations (Fig. 4). The size of fish captured in PM traps showed marked oscillations in the three dominant species, clearly following the appearance of juvenile individuals in the cases of toothcarp and loach. The mean size of fish caught in the different surveys in PM traps and in F1 nets was positively correlated for toothcarp (r = 0.86; P < 0.01; n = 11) and sand smelt (r = 0.91; P < 0.01; n = 10), but this relation was not significant in the case of loach (r = 0.42; P = 0.17; n = 12). No other pair-wise correlation between sizes of fish captured in different trap types resulted statistically significant for any species. 4. Discussion The results of this study clearly show that the use of different passive methods produce different results in relation to fish community and population structure characteristics. The most important differences in the taxonomic composition of captures were those observed between PM traps and F2 nets. These traps were the only ones that capture certain species or size classes. Thick-lipped grey mullets were caught exclusively in F2 nets and common gobies, black-stripped pipefish and glass eels were exclusively caught in PM traps. There were important differences in the size of captured toothcarp among the different trap types. The smallest toothcarp individuals were only caught in PM traps. The length-frequency distribution from PM trap catches Fig. 4. Variation in the mean size (±S.E.) of toothcarp, loach and sand smelt during the study period as recorded from catches in the four trap types. PM traps—solid circles, solid line; MM traps—solid triangles, solid line; F1 nets—empty circles, dotted line; F2 nets—empty triangles, dotted line. resembled that previously recorded by other authors (Fernández-Delgado et al., 1988), but all other trap types failed to catch the smallest toothcarp size classes. In fact, though overall efficiency at capturing toothcarp was higher for F1 nets than for PM traps, this difference tended to disappear in summer surveys, due to the abundant catches of juvenile fish in PM traps, which were no caught in F1 nets (see Fig. 4). Working with mosquitofish (Gambusia affinis Baird and Girard 1853), Blaustein (1989) also noted that the efficiency of minnow traps, which we equivalate with our MM traps, was greater for large individuals (>35 mm TL) than for small ones. After these and our results, large-meshed traps would not be an appropriate methodology to assess population structure or to compare densities among habitats or populations when studying toothcarp or similar small fish species. Sand smelt captures were much greater in F1 nets than in any other trap type. Since sand smelt is a schooling species (Vizzini and Mazzola, 2002) the relatively large interception area of F1 traps (see Table 1) would facilitate the entrance of whole schools in to the trap. The large efficiency differences between F1 nets and PM traps could also be explained if sand smelt occupied positions within the water column above those used by toothcarp. PM traps exclusively sample fish moving at 9 cm or less from the stream bottom, while fish swimming up to 30 cm from the bottom could enter F1 nets. The net wings in fyke nets may also direct pelagic fish schools to the net’s funnel, notably amplifying their interception area. Moreover, PM traps were unable to capture large sand smelt individuals (e.g. Leonardos and Sinis, 2000), which could be caught in other trap types (see Table 5). These differences at catching large individuals could not be explained by the use of different mesh sizes, and should be related to interception areas. F1 trap was also the most efficient method in capturing loach, a pattern that was consistently observed during the study period. However, loach has special features which can largely influence its catches in different trap types. It is a bottom dwelling species that can actively pass its body through mesh openings, being able to bury itself in fine sand, as has been reported for other Cobitis (e.g. Robotham, 1978). This meant that, except for PM traps, we could never be sure that a certain loach had entered a trap through the funnel. In fact, MM traps and both fyke nets often functioned as gill-nets, retaining loaches that were either entering or leaving the traps through the mesh (both possibilities were observed in the field, though not quantified). Since gillnetting is very size selective (Hubert, 1996), this resulted in the narrow size ranges of loach sizes captured in F1 nets and MM traps. Lateral captures and escapes were not quantifiable, and thus loach capture efficiency comparisons between trap types could be meaningless. These fish entanglements could also accentuate the injuries produced by traps and would potentially increase post release mortality (Cooke et al., 1998). PM traps can be thus considered the most accurate to sample loach among the tested traps, since all captured fish entered the trap through the funnel, the whole size range was covered by captures in these traps (Table 3) and PM traps were the only trap type that accurately reflected the temporal variation in size structure (Fig. 4). Moreover, PM traps allowed the capture of small sized loaches that had not been previously taken in other population studies (e.g. Soriguer et al., 2000; Oliva-Paterna et al., 2002). Apart from efficiency and selectivity, other factors could influence the use of one or another trap type. Shoup et al. (2003) advised against the value of comparing population or community structure data that had been obtained by different passive methods. PM traps are the most easily repeatable, as well as the cheapest, among the four trap types employed. Moreover, due to their small size and reduced weight many traps can be set by a single operator. The precision of microhabitat characterisation around traps would also differ among trap types, since microhabitat complexity increased along with increasing intersection area. Thus, the small intersection area of PM traps allows a precise description of the environmental conditions around the funnel (Clavero et al., 2005). In contrast, the other traps have large intersection areas (and in the case of fyke nets also a lead directed to the funnel), making it difficult to interpret possible catch variations across microhabitats. 5. Conclusions No one single trap type was adequate for sampling all fish species and sizes in the study area. Different traps sampled different microhabitats, resulting in clear differences in the composition of catches. PM traps are efficient at capturing bottom dwelling or small, benthic associated species (i.e. loach and toothcarp) but fail to efficiently sample schooling or more pelagic species (i.e. sand smelt), or large individuals of most species. F1 nets are the most efficient trap type when considering all fishes together and works better than any other method to survey sand smelt populations, but do not accurately catch benthic species like loach. Trap efficiency was influenced both by mesh size (small meshed traps being more efficient) and interception area (large interception areas allowing more efficient sampling of pelagic species). Finally, our results show that sequential trapping along annual cycles can reveal life-history progression for some species, though this sampling implies the use of appropriate gears for each particular species. Acknowledgments Dr. Michael G. Fox and two anonymous referees provided very helpful comments on early versions of the manuscript. We greatly acknowledge the assistance and company during the field work provided by Leonardo Fernández, Marta Narváez, Luis Barrios, Jose Á lvarez, Eduard Deuan, Laura and Eli. This study is part of the project “Biotic integrity and environmental factors of watersheds in south-western Spain. Application to the management and conservation of Mediterranean streams” (Ministerio de Ciencia y Tecnologı́a, REN2002-03513/HID). References Blaustein, L., 1989. 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