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Nursery use of shallow habitats by epibenthic fishes in Maine nearshore waters
Estuarine, Coastal and Shelf Science 56 (2003) 73–84
Nursery use of shallow habitats by epibenthic fishes in Maine nearshore waters M.A. Lazzari*, S. Sherman, J.K. Kanwit Maine Department of Marine Resources, P.O. Box 8, West Boothbay Harbor, ME 04575, USA Received 4 June 2001; received in revised form 10 December 2001; accepted 10 December 2001
Abstract Species richness and abundance of epibenthic fishes were quantified with daytime beam trawl tows in shallow water habitats during April–November 2000 of three mid-coast Maine estuaries; Casco Bay, Muscongus Bay and the Weskeag River. Five shallow (<10 m) habitats were sampled, Zostera marina, Laminaria longicruris, Phyllophora sp., Microciona prolifera and unvegetated sandy areas. Thirty-two species of fishes were collected. Species richness tow1 was greater in Casco Bay followed by the Weskeag River and Muscongus Bay respectively. Catch per unit effort (CPUE) of fishes was greater in Casco Bay than in the Weskeag River or Muscongus Bay. Species richness and faunal abundances were positively associated with vegetation, particularly Zostera, at all sampling locations. CPUEs of fishes were higher in Zostera due primarily to the abundance of Gasterosteus aculeatus, Apeltes quadracus, Pungitius pungitius, Myoxocephalus aenaeus, and Cylcopterus lumpus. The fish community of mid-coast estuaries was dominated by young-of-the-year (YOY) and juvenile fishes and all of the habitat types function as nursery areas. Twelve species (38%) of commercial and recreational importance were collected in the three estuaries, but the percentage was higher in Casco Bay (44%) and the Weskeag River (46%). These species included Anguilla rostrata, Clupea harengus, Gadus morhua, Microgadus tomcod, Pollachius virens, Urophycis chuss, Urophycis regia, Urophycis tenuis, Osmerus mordax, Macrozoarces americanus, Tautogolabrus adspersus, and Pleuronectes americanus. Four species, G. morhua, M. tomcod, P. virens, and U. tenuis were more common in spring than summer or autumn. Pleuronectes americanus was most abundant in summer followed by spring and autumn respectively. This study documents the importance of shallow estuarine areas in Maine as nurseries for these species. 2003 Elsevier Science B.V. All rights reserved. Keywords: Zostera; Community composition; Maine coast; Estuarine fauna
1. Introduction The fish fauna of the deeper areas of the Gulf of Maine (GOM) system was well described (Bigelow & Schroeder, 1953), and published studies on shallow water fish communities in the region exist for Passamaquoddy Bay (MacDonald, Dadswell, Appy, Melvin, & Methven, 1984; Tyler, 1971), Penobscot Bay (Lazzari & Tupper, 2002), the Sheepscot River (Recksiek & McCleave, 1973), Montsweag Bay (Targett & McCleave, 1974), Sagadahoc Bay (Lazzari et al., 1999) and Wells Harbor (Ayvazian, Deegan, & Finn, 1992). The majority of these fish
* Corresponding author. E-mail address: [email protected] (M.A. Lazzari).
community studies were relatively short term (Ayvazian et al., 1992; Recksiek & McCleave, 1973; Targett & McCleave, 1974; Tyler, 1971), often lasting a year or less. Many were close to 30 years old and provide little information on the basic ecology of recreational and commercial finfish species. Recent impacts of intensive human development of the shore-line and increased exploitation of the fisheries stocks on species composition, abundance and habitat use by many recreationally and commercially important species were unknown. In order to effectively manage marine recreational and commercial finfish species such as Pleuronectes americanus, Gadus morhua, and Pollachius virens, information was needed on the distribution, abundance, and habitat requirements of the juvenile stages of these species in shallow habitats. The 1996 amendments to the
0272-7714/03/$ - see front matter 2003 Elsevier Science B.V. All rights reserved. doi:10.1016/S0272-7714(02)00122-1
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Magnuson–Stevens Fishery Conservation and Management Act, known as the Sustainable Fisheries Act (SFA), emphasized the importance of habitat protection to healthy fisheries and strengthened the ability of the National Marine Fisheries Service (NMFS) and the regional fishery management councils to protect and conserve essential marine, estuarine, and anadromous fish habitat. Information on the nearshore distribution of epibenthic fishes was important due to the nursery function of shallow inshore habitats, the environmental variability of these areas, and the high potential for anthropogenic impact (Brown & McLachlan, 1990; Kneib, 1997; MacDonald et al., 1984; Warfel & Merrimen, 1944). The importance of vegetation, particularly Zostera marina and other seagrasses as epibenthic fish habitat has been demonstrated outside the GOM (Heck, Able, Fahay, & Roman, 1989; Huh, 1984; Paterson & Whitfield, 2000; Sogard & Able, 1991; Sogard, Powell, & Holmquist, 1987; Szedlmayer & Able, 1996; Weinstein & Brooks, 1983) with higher faunal densities found in seagrass relative to unvegetated sand or mud substrates (see review in Orth, Heck, & van Montfrans, 1984). Seagrass functions as nursery habitat for newly settled juvenile fishes and decapods (Adams, 1976; Bell & Pollard, 1989; Heck et al., 1989; Heck & Thoman, 1984; Orth & van Montfrans, 1987) and has a demonstrated value as a refuge from predation (Heck & Thoman, 1981; Heck & Wilson, 1987; Kneib, 1987; Leber, 1985; Paterson & Whitfield, 2000; Stoner, 1982; Wilson, Heck, & Able, 1987). However, many studies have been restricted to a single habitat and very few compared ichthyofaunal utilization of different habitats within the same estuary. The purpose of this study was to determine the species composition and relative abundance of epibenthic fishes, particularly juvenile forms of marine recreational and commercial species (Gadus morhua, Microgadus tomcod, Pollachius virens, Urophycis chuss, U. tenuis, Osmerus mordax, Tautogolabrus adspersus, and Pleuronectes americanus) and their habitats in the shallow (<10 m) waters of mid coastal Maine estuaries by (1) documenting their seasonal presence and relative abundance and (2) relating their occurrence to habitat through beam trawl sampling.
2. Materials and methods 2.1. Study area Three estuaries with Zostera marina (eelgrass) present and located in mid coastal Maine (Casco Bay, Muscongus Bay, Weskeag River) were sampled in this study (Fig. 1). The Cousins Island area of Casco Bay (7015¢, 4378¢) was characterized by low relief, moderate
Spartina alterniflora salt marsh, expansive areas of Zostera and adjacent mudflat and mussel areas. Freshwater input from the Royal River was moderate though surface salinities were high (>25 PSU) with the exception of station 1 following rainfall. Tides were semidiurnal and in the 2.4–3.2 m range. The Muscongus Bay estuary (longitude 6940¢, latitude 4395¢) was characterized by moderate relief, minimal saltmarsh and large areas of mudflat. Freshwater input from the Medomak River was low and salinities were high. Tides were semidiurnal and range from 2.5–3.3 m and discrete areas of submerged aquatic vegetation (Zostera, Laminaria longicruris, kelp and Phyllophora sp., algae) were present. The Weskeag River estuary (6920¢, 4398¢) was distinguished by moderate relief, nominal salt marsh but expansive mudflat and mussel areas. Freshwater input was minimal and salinities were always high. Tides were semidiurnal and ranged from about 2.5–3.5 m and large areas of aquatic vegetation (Zostera and Laminaria) were present. 2.2. Field methods Sampling for juvenile fishes in shallow subtidal habitats in mid-coast coast estuaries began in early April and continued into November 2000. Ten stations with towable bottom were selected and sampled bimonthly during daylight hours in Muscongus Bay and the Weskeag River and 11 stations were sampled in Casco Bay. All stations sampled were between one and 10 m in depth. At each station, one 5 min tow was made with a small beam trawl (2.0 · 0.5 m opening, 3 mm codend mesh). Samples were sorted live and discarded except for species of particular interest which were preserved in 10% formalin. All fishes were identified, counted and measured for total length (cm). Surface temperature and salinity by refractometry were recorded at each site and depth was measured using a hull mounted electronic depth finder. 2.3. Statistical analyses Fish catches were expressed as number tow1 (CPUE) for the beam trawl samples. All statistical testing used SYSTAT statistical software (Wilkinson, 1996). Our primary objective was to identify patterns of species associations in several habitats. The method traditionally used in fish-community studies to identify groups of species or stations has been cluster analysis, usually using an agglomerative clustering algorithm. This method produces a classification diagram (dendrogram), which also shows the hierarchical relationships between groups. Patterns of occurrence were tested using cluster analysis (CA) and multidimensional scaling (MDS, Field, Clarke, & Warwick, 1982). In each
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Fig. 1. Station locations in mid-coast Maine estuaries (Casco Bay, Muscongus Bay and the Weskeag River) sampled with beam trawl from April through November 2000.
analysis, samples taken at each station were combined and rare fish species (3 individuals caught during the entire study) were excluded. The among station similarity matrix was computed using CPUE data that were root–root transformed in order to reduce the influence of the most abundant species and association matrices were produced using Bray–Curtis similarity measures. CA were prepared for each estuary separately while MDS was performed with all stations combined. Secondly, to compare species number tow1 and CPUE of the fishes across the various estuaries and habitats, one-way analyses of variance (ANOVA) testing followed by a priori SD (least significant difference) (LSD) multiple comparisons tests or two-sample t-tests were used when the data met the assumptions of normality and heterogeneity of variance, following the method of means testing outlined by Sokal and Rohlf (1981). Species richness and CPUEs (including all sampling dates) were compared for the three estuaries using ANOVA for unbalanced designs. Additional ANOVAs (unbalanced designs) of species richness and CPUE were run for three depth ranges (0–3 m, 3–6 m, 6–10 m) and for three seasons [spring (April–June),
summer (July–September), and autumn (October–November)]. All numbers were log10 transformed prior to analysis. Although concerns for experimental error rate exist when multiple comparisons were made in a given study, the objective of this study was to make a series of individual comparisons. Due to the robustness of ANOVA and the highly significant differences among groups (P < 0:001 for the overall ANOVA for most tests), the results of the ANOVA’s and planned comparisons could be interpreted reliably. Two-sample t-tests for unequal variances (Sokal & Rohlf, 1981) were used to determine whether means of species richness and CPUE of all species differed between Zostera and unvegetated sandy habitats in each estuary. Two-sample t-tests for unequal variances (Sokal & Rohlf, 1981) were also used to determine whether means of CPUE of individual species differed between Zostera and unvegetated sandy habitats. These comparisons were designed to determine the relative value (in terms of mean species richness or CPUE) of the different habitats for the common epibenthic fishes and the eight target species. These multiple comparisons provided a general view of habitat relationships since it was not possible to directly
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compare each habitat without there being some influence of site location within the estuary because the same substrate types did not occur at all sites.
3. Results 3.1. Site characteristics Surface salinities differed little among sites in the Weskeag River and Muscongus Bay ranging from 28 to 33 PSU from April through November while salinities in Casco Bay were more variable, ranging from 22 to 31 PSU. On average, the maximum difference in salinity across all sites within an estuary was <5 PSU with the only exception being Casco Bay station 1 (18 PSU). Surface water temperatures were similar among the three estuaries with slightly warmer water (1–2 C) occurring in Casco Bay. Water temperatures everywhere increased from a minimum of 6 C in April to a maximum of 17 C in late July before dropping gradually during the autumn. By November, temperatures averaged about 9 C. Little variation was
observed in water temperatures among stations within each estuary during any sampling period (<2 C). Vegetation was a widespread habitat component in Casco Bay and in the Weskeag River relative to Muscongus Bay. Zostera marina (eelgrass) occurred at four stations in Casco Bay and the Weskeag River, but only at two stations in Muscongus Bay. Laminaria longicruris (kelp) occurred at one station in the Weskeag River and occasionally in Casco and Muscongus Bays as did Phyllophora sp. (algae) in Muscongus Bay. Microciona prolifera (sponge) occurred consistently at one station sampled in Casco Bay. A total of 416 beam trawl tows were collected in Casco Bay (n ¼ 147), Muscongus Bay (139) and the Weskeag River (130) (Table 1). Depending on the weather, the number of stations sampled on a sampling trip varied from 6–12 in Casco Bay, 6–13 in Muscongus Bay and 4–11 in the Weskeag River. The fewest number of tows were made in April (16) while the highest number were collected in late July and early August (34). By habitat, more tows were made on sandy substrate (236) than were made in areas vegetated with Zostera (134), Laminaria (34), in Microciona (10) or
Table 1 Sampling effort, species richness (total and mean SE species per tow), and CPUE (mean SE number per tow) for stations in Casco Bay, Montsweag Bay and the Weskeag River, Maine. Vegetation (veg.) Psp ¼ Phyllophora sp.; Zm ¼ Zostera marina; Ll ¼ Laminaria longicruris; Mp ¼ Microciona prolifera Estuary
Station (veg.)
Number of tows
Total species
Mean species per tow
Mean CPUE
Casco Bay
1 2 3 4 5 6 7 8 9 10 11
(Zm) (Mp)
13 13 14 13 14 14 14 12 13 14 11
13 11 18 17 18 16 17 9 10 19 12
3.7 0.5 2.9 0.4 4.3 0.7 6.2 0.7 6.1 0.6 3.0 0.5 4.0 0.6 2.4 0.3 2.9 0.4 6.9 0.5 3.1 0.5
10.6 3.1 9.4 2.6 13.5 2.7 66.9 16.5 48.9 10.0 9.3 2.4 16.6 6.1 6.7 1.9 10.0 2.3 74.7 19.9 9.1 2.5
Montsweag Bay
1 (Zm) 2 3 4 (Psp) 5 6 7 (Zm) 8 9 10
13 12 14 12 13 13 13 13 11 11
13 10 10 14 11 9 13 9 15 9
4.0 0.5 3.2 0.5 2.4 0.3 3.5 0.5 2.2 0.4 2.7 0.4 4.9 0.5 2.2 0.3 3.5 0.5 2.4 0.4
34.9 18.2 11.4 2.6 6.8 1.3 14.9 4.8 6.7 0.9 3.3 0.6 22.3 3.9 12.6 2.6 12.6 3.4 5.6 1.9
Weskeag River
1 2 3 4 5 6 7 8 9 10
14 13 14 14 13 11 14 13 11 10
10 7 13 17 11 9 15 13 15 3
2.4 0.4 1.9 0.3 3.5 0.4 4.1 0.5 2.8 0.2 2.1 0.3 5.5 0.8 4.2 0.6 5.6 0.4 1.5 0.2
4.1 1.2 4.9 1.4 6.4 1.7 10.4 2.9 6.7 1.0 7.0 1.9 27.3 11.3 85.1 26.7 41.2 13.1 2.5 0.5
(Zm) (Zm) (Zm)
(Ll) (Zm)
(Zm) (Zm) (Zm)
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Phyllophora (2) (Table 1). In all three estuaries, more tows were made in sandy than in vegetated areas.
richness and abundance were greatest at the stations where Zostera was present regardless of estuary.
3.2. Species richness
3.3. Habitat selection
A total of 32 species were collected in the three estuaries with a similar number in each estuary, 25 species in Casco Bay, 24 in Muscongus Bay and 22 in the Weskeag River. However, overall species tow1 was significantly greater in Casco Bay followed by the Weskeag River and Muscongus Bay respectively (ANOVA, F2;413 ¼ 19:2, P< 0.001). The fish fauna was dominated by a relatively few species, but the temporal and habitat patterns of species richness varied. Apeltes quadracus (fourspine stickleback), Pungitius pungitius (ninespine stickleback), Myoxocephalus aenaeus (grubby), Gasterosteus aculeatus (threespine stickleback), and Pleuronectes americanus (winter flounder), made up 73% of the total fishes collected. Twelve commercial and recreational species, including six gadoid species were collected. These included Anguilla rostrata (American eel), Clupea harengus (Atlantic herring), Gadus morhua (cod), Urophycis tenuis (white hake), U. regia (spotted hake), U. chuss (red hake), Pollachius virens (pollock), Microgadus tomcod (tomcod), Tautogolabrus adspersus (cunner), Macrozoarces americanus (ocean pout), Osmerus mordax (rainbow smelt) and Pleuronectes americanus (winter flounder). Seventeen species occurred in all three estuaries including eight commercial and recreational species. Five species were represented by a single individual including Fundulus heteroclitus (mummichog), Ulvaria subbifurcata (radiated shanny), Myoxocephalus scorpius (shorthorn sculpin), M. octodecimspinosus (longhorn sculpin) and Dactylopterus volitans (flying gurnard). Two of the most abundant species (M. aenaeus and P. americanus) were widely distributed in the three estuaries (Table 2). Myoxocephalus aenaeus and P. americanus occurred in more tows (>50%) than any other species. Syngnathus fuscus (northern pipefish), Pholis gunnellus (rock gunnel) and Cyclopterus lumpus (lumpfish) all occurred in greater than 20% of the tows. G. morhua, U. tenuis, U. chuss, P. virens, M. tomcod, and T. adspersus occurred in 9–14% of tows while O. mordax were in 5%. Six species (G. morhua, U. tenuis, T. adspersus, P. gunnellus, M. aenaeus, P. americanus) occurred in all five habitats sampled (Table 2); five other species occurred in all habitats except Phyllophora. Seven species occurred in a single habitat, usually sand. Clupea harengus, M. tomcod, U. regia, and M. americanus were not present in all estuaries. The total number of species was highest on sand (29) followed by Zostera (26), Laminaria (16), Microciona (13), and Phyllophora (10). The high species number observed in unvegetated sandy areas was due to increased sampling effort that resulted in the collection of uncommon species such as the Myoxocephalus species. However, mean fish species
Species richness by station (Fig. 2a) was generally highest in Zostera in Casco Bay (stations 4, 5, 10), Muscongus Bay (stations 1, 7) and the Weskeag River stations (4, 7, 8, 9). However, station 7 in Zostera in Casco Bay was an exception. More species generally occurred at stations 4 and 9 in Muscongus Bay where Phyllophora or Laminaria was sometimes encountered and in the Weskeag River where Laminaria (station 3) occurred. CPUE (Fig. 2b) followed the same pattern, being highest at stations with Zostera in all three estuaries. The results of cluster analyses (CA) classified the Casco Bay, Muscongus Bay and Weskeag River stations into habitat groups based on species richness (Fig. 3). A major dichotomy classified three stations (4, 5, 10) in Casco Bay (Fig. 3a) located in shallow Zostera and possessing the greatest species diversity from the eight remaining stations with fewer species present. Two other stations, one in a channel area (3) and another in sparse Zostera (7) were joined next to last. The deepest site (station 8) in Casco Bay had low CPUE and species diversity. Similar trends were revealed in the cluster analyses of stations in Muscongus Bay (Fig. 3b) and the Weskeag River (Fig. 3c). The deepest station in Muscongus Bay (6) and in the Weskeag River (10) also had low diversity and CPUE and were the last stations added to their respective dendrograms. The two stations with Zostera (1, 7) in Muscongus Bay were the next least similar to the other sites, followed by station 9 where Zostera was present in two tows. In the Weskeag River (Fig. 3c). three shallow stations with Zostera (7, 8, 9) were joined next to last, preceded by another station where Zostera occurred, station 4. Non-metric multidimensional scaling analysis (MDS) of the mid coast fish data also grouped individual stations based on habitat and species number similar to the cluster analysis results (Fig. 4). The shallow stations with Zostera in Casco Bay (4, 5, 10), in Muscongus Bay (1, 7) and in the Weskeag River (4, 7, 8, 9) were grouped together. However, one station in sparse Zostera in Casco Bay (station 7) was placed into the larger grouping of stations located primarily on sandy substrates. Six of the remaining stations with low species richness formed a grouping bounded by the stations in deepest water in each estuary (c8, m6, w10). In summary, the two multivariate methods generally grouped stations with Zostera together. 3.4. Abundance A total of 7300 fishes (32 species) were collected with the beam trawl. Total abundance was greater in Casco
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Table 2 Fishes (n ¼ 32 species), CPUE (number tow1) and percent frequency of occurrence collected in shallow habitats in mid-coast Maine estuaries with 2.0 m beam trawl from April to November 2000. Estuaries are Casco Bay (CB), Muscongus Bay (MB), Weskeag River (WR). Habitats are Phyllophora sp. (Psp), Zostera marina (Zm), Laminaria longicruris (Ll), Microciona prolifera (Mp) and sand (S); p ¼ present Estuary
Habitat
Family species effort
Common name
CB 147
MB 139
WR 130
Psp 2
Zm 134
Ll 34
Mp 10
Sand 236
Anguilla rostrata
American eel
Clupea harengus
Atlantic herring
Osmerus mordax
Rainbow smelt Atlantic cod
Microgadus tomcod
Atlantic tomcod
Pollachius virens
Pollock
Urophycis chuss
Red hake
Urophycis regia
Spotted hake
Urophycis tenuis
White hake
Macrozoarces americanus
Ocean pout
Fundulus heteroclitus
Mummichog
Menidia menidia
Atlantic silverside
Apeltes quadracus
Fourspine stickleback
Gasterosteus aculeatus
Threespine stickleback
Gasterosteus wheatlandi
Blackspotted stickleback
Pungitius pungitius
Ninespine stickleback
Syngnathus fuscus
Northern pipefish
Tautogolabrus adspersus
Cunner
Lumpenus maculates
Daubed shanny
Ulvaria subbifurcata
Radiated shanny
Pholis gunnellus
Rock gunnel
Hemitriperus americanus
Sea raven
Myoxocephalus aenaeus
Grubby
M. octodecimspinosus
Longhorn sculpin
M. scorpius
Shorthorn sculpin
Cylcopterus lumpus
Lumpfish
Liparis atlanticus
Seasnail
Liparis coheni
Gulf seasnail
L. liparis
Striped seasnail
Dactylopterus volitans
Flying gurnard
<0.1 1 — — 0.1 2 0.3 9 — — 0.3 9 0.2 14 — — 0.3 10 <0.1 1 — — — — 3.1 8 0.2 7 — — <0.1 1 0.3 19 0.3 18 <0.1 1 <0.1 1 0.5 28 <0.1 1 3.1 54 <0.1 1 <0.1 1 0.2 9 — — — — <0.1 1 <0.1
<0.1 1 — — <0.1 1 0.4 11 0.3 12 0.3 13 0.4 16 0.1 5 0.6 25 — — — — — — <0.1 1 1.7 15 — — 8.4 22 0.2 12 0.1 9 — — — — 0.3 22 0.1 4 1.4 44 — — — — 1.1 36 <0.1 1 <0.1 2 <0.1 1 —
— — — — — — 4.0 p — — 1.5 p — — — — 3.0 p 1.0 p — — — — — — — — — — — — — — 0.5 p — — — — 1.5 p 0.5 p 27.5 p — — — — — — — — — — — — —
<0.1 1 <0.1 2 0.2 9 0.4 10 0.9 23 1.1 25 0.2 13 <0.1 3 0.5 19 <0.1 1 — — <0.1 3 13.8 41 6.1 53 <0.1 2 8.7 35 1.1 36 0.6 23 <0.1 1 — — 0.4 25 0.2 7 4.0 77 — — — — 1.2 44 <0.1 1 <0.1 1 — — —
— — — — — —
Gadus morhua
<0.1 1 <0.1 2 0.4 12 0.1 6 0.7 17 0.5 12 0.1 8 — — 0.1 8 <0.1 2 <0.1 1 <0.1 3 10.1 46 4.0 34 <0.1 3 0.7 16 1.2 42 0.4 14 <0.1 1 — — 0.2 14 0.2 8 2.2 57 — — — — 0.5 18 <0.1 1 — — — — —
— — — — 0.4 p 0.4 p — — — — 0.7 p — — 0.1 p — — — — — — 0.5 p — — — — — — 0.5 p 0.5 p — — — — 0.2 p 0.1 p 0.9 p — — — — 0.1 p — — — — — — —
<0.1 <1 — — 0.2 4 0.1 6 0.1 4 0.1 3 0.2 9 <0.1 1 0.2 9 <0.1 <1 <0.1 <1 <0.1 <1 0.3 9 <0.1 3 <0.1 <1 <0.1 3 0.4 21 0.1 8 <0.1 1 — — 0.3 17 <0.1 3 1.2 36 <0.1 <1 <0.1 <1 <0.1 7 — — <0.1 <1 <0.1 <1 <0.1
0.5 21 <0.1 3 0.3 15 0.4 26 — — 0.5 24 — — — — — — 0.1 6 — — — — <0.1 3 0.1 15 0.1 12 — — <0.1 3 0.5 35 — — 1.8 56 — — — — 1.0 29 <0.1 3 — — — — —
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M.A. Lazzari et al. / Estuarine, Coastal and Shelf Science 56 (2003) 73–84 Table 2 (continued ) Estuary Family species effort
Common name
Scopthalmus aquosus
Windowpane
Pleuronectes americanus
Winter flounder
Total species
CB 147 — 0.2 8 2.5 63 25
Habitat MB 139 1 0.1 6 1.9 46 24
Bay (n ¼ 3576) and the Weskeag River (2159) than in Muscongus Bay (1565). Dominant fishes were similar among estuaries with mean CPUE of A. quadracus, P. pungitius, M. aenaeus, G. aculeatus, and P. americanus about 2–5 individuals tow1 (Table 2). Apeltes quadracus, G. aculeatus, P. americanus and M. aenaeus comprising about 67% of the fishes collected in Casco Bay and A. quadracus, M. aenaeus, and P. americanus comprised about 70% of the fishes were collected in Muscongus Bay. In the Weskeag River, P. pungitius replaced A. quadracus as a dominant species and with G. aculeatus, P. americanus and C. lumpus made up about 80% of the fish abundance collected there. CPUE for all species was significantly greater (ANOVA, F2;413 ¼ 8:2, P < 0.001) in Casco Bay (24.3) compared with either the Weskeag River (16.6) or Muscongus Bay (11.3). Differences in CPUE existed by habitat within each system (Table 2). Fish CPUEs in Zostera within Casco Bay and the Weskeag River were about 12 times higher than in nearby unvegetated areas. In Casco Bay, most target species were more abundant in Zostera while in the other three habitats, P. americanus and O. mordax were more common. All of the target species in the Weskeag River were more abundant in Zostera although U. tenuis was common in Laminaria as well. Fish CPUE
Fig. 2. Mean number of fish species tow1 (a) and Catch per unit effort (number tow1) (b) of fishes collected by station with 2.0 m beam trawl in Casco Bay (CB), Muscongus Bay (MB) and the Weskeag River (WR) from April through November 2000. (*¼ Zostera present, ¼ uncommon habitat, see Table 1). r CB; h MB; M WR.
WR 130
Psp 2
Zm 134
Ll 34
Mp 10
Sand 236
— <0.1 1 1.2
— — — 1.5
— <0.1 1 1.6
— <0.1 3 1.6
— 1.4 p 3.1
<1 0.1 6 2.0
55 26
44 16
39 22
p 10
p 13
46 29
was six times higher in Zostera in Muscongus Bay but was greatest in the two tows made in Phyllophora. Of the target species collected in Muscongus Bay, P. virens, U. tenuis and T. adspersus were more abundant in Zostera and Phyllophora while U. chuss was more abundant in sandy areas. Gadus morhua and P. americanus were about equally abundant among the four habitats sampled. Fish CPUEs in Laminaria and Microciona within Casco Bay and in Laminaria within the Weskeag River, were also higher than tows in nearby unvegetated areas. Most of the fish species collected in this study were represented by young-of-the-year (YOY) and juveniles with the exception of winter flounder. Length frequencies of the eight common recreational and commercial species revealed all total lengths (TL) of G. morhua (mean=5.0, SD=0.5) and T. adspersus were less than 10 cm (4.4, 0.3). Five other species never exceeded 19 cm TL, including P. virens (mean=5.0, SD=0.4), O. mordax (6.3, 0.5), M. tomcod (7.4, 0.3), U. tenuis (8.3, 0.6), and U. chuss (9.3, 0.6); Pleuronectes americanus ranged from 1–42 cm TL, with most (63%) between 2 and 10 cm and a second group occurred at 12–16 cm (20%). Eleven P. americanus were greater than 20 cm. 3.5. Habitat comparisons Fish species richness tow1 and CPUE were higher for Zostera versus unvegetated sandy habitat. Overall species richness tow1 was positively associated with Zostera (two sample t-test, t ¼ 12:7, P < 0:001) as was total CPUE (two sample t-test, t ¼ 6:7, P < 0:001). Within all estuaries, greater species diversity and CPUE also occurred in Zostera relative to unvegetated areas (all two sample t-tests, t > 3:3, P < 0:001 except for CPUE in Muscongus Bay where t ¼ 2:4, P < 0:05). In individual species testing, CPUE of eight fishes (G. morhua, M. tomcod, G. aculeatus, A. quadracus, P. pungitius, C. lumpus, H. americanus, M. aenaeus) were significantly higher in tows in Zostera (all two sample t-tests, t > 2:0, P < 0:05) than unvegetated tows. CPUE of P. americanus was higher over sand (two sample t-test, t ¼ 2:2, P < 0:05). Percent total CPUE of the eight common target species ranged from 22 to 87% in Zostera and four species (U. tenuis, G. morhua, U. chuss, P. americanus)
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Fig. 4. Multidimensional scaling (MDS) of the fish samples caught by station with beam trawl in mid coast Maine estuaries from April through November 2000. The Casco Bay stations (c) were numbered 1–11 and stations in Muscongus Bay (m) and the Weskeag River (w) were numbered 1–10. (Zostera present at underlined stations, * ¼ uncommon habitats).
Fig. 3. Cluster analysis dendrograms of the fish samples collected by station with beam trawl in Casco Bay (a), Muscongus Bay (b) and the Weskeag River (c) from April to November 2000. (Zostera present at underlined stations, * ¼ uncommon habitats.)
also were common (>25%) in Laminaria. Osmersus mordax, U. chuss, T. adspersus, P. americanus, and G. morhua were common in the two rare habitats (Phyllophora sp. and Microciona) while on sandy habitats, P. americanus and O. mordax were common. 3.6. Seasonal and depth differences Species richness and CPUE showed peaks in late June/July and in September/October in the three estuaries. However, analyses of the mean number of
species tow1 for season for each estuary revealed that there were significantly more species of fishes present in spring (April–June) than in autumn (October–November) only in Casco Bay (ANOVA, F2;144 ¼ 3:03, P < 0:05). Species number was similar among seasons in Muscongus Bay and the Weskeag River. Similar analyses of mean CPUE of fishes for season in each estuary revealed that were there significantly more fishes present in summer (July–September) than in autumn (October–November) only in the Weskeag River (ANOVA, F2;127 ¼ 4:71, P < 0:01) with similar CPUEs among seasons in Casco and Muscongus Bays. The occurrence of several target species was seasonal with four gadoid species collected primarily in spring (April–June). Gadus morhua (two sample t-test, t ¼ 3:71, P < 0:001) and P. virens (two sample t-test, t ¼ 3:61, P < 0:001) were more abundant during spring as were U. tenuis (ANOVA, F2;65 ¼ 5:80, P < 0:01) and M. tomcod (ANOVA, F2;41 ¼ 7:56, P < 0:001). Others had a more protracted occurrence in our collections with T. adspersus collected during all sampling periods with a September peak, U. chuss and O. mordax abundances peaked in late June–July and August, respectively. Pleuronectes americanus were almost always present but CPUE was highest from late June through October. Pleuronectes americanus were significantly more abundant during summer compared with spring which in turn was greater than autumn (ANOVA, F2;201 ¼ 7:42, P < 0:001). CPUEs of T. adspersus, U. chuss and O. mordax were about equal during the three seasons.
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The overall number of fish species and CPUE differed by depth. More fish species tow1 (ANOVA, F2;413 ¼ 46:4, P < 0:001) were collected at the shallowest depths (between 0.6 and 3 m) followed by intermediate depths (to 6 m) when compared with deeper areas. Overall CPUE for all fishes was highest in shallower water as well (ANOVA, F2;413 ¼ 21:3, P < 0:001). However, CPUE’s of each target species were not significantly different by depth with the exception of T. adspersus which were more abundant in water less than 3 m (ANOVA, F2;59 ¼ 3:98, P < 0:05).
4. Discussion Vegetation was an important component of habitat quality in shallow Maine estuaries. The presence of vegetation, particularly Zostera marina and Laminaria longicruris, had a positive effect on fish species richness and abundance in mid-coast coast estuaries. Casco Bay and the Weskeag River where more vegetated habitats occurred had significantly more fish species tow1 and higher abundances than Muscongus Bay where more unvegetated sandy substrates were present. In all three estuaries, total fish species tow1 and abundances were generally higher in Zostera than nearby unvegetated sandy areas. These findings were consistent with results of other investigations where a more diverse fish community and greater abundance occurred in vegetated areas (Heck et al., 1989; Lazzari & Tupper, 2002; Nixon & Oviatt, 1973; Paterson & Whitfield, 2000; Pearcy & Richards, 1962; Sogard & Able, 1991; Sogard et al., 1987; Szedlmayer & Able, 1996). Laminaria in the Weskeag River and Muscongus Bay also had a positive effect on species richness and abundance but published information does not exist for comparison in this habitat. A number of dominant taxa exhibited clear habitat preferences although there were a few generalist species (i.e. P. gunnellus, P. americanus) that occurred over a variety of substrates. The three Gasterosteid species appeared more restricted in the habitats they utilize to three-dimensional structure such as Zostera and were virtually absent at other habitats. Syngnathus fuscus, T. adspersus, M. aenaeus, and C. lumpus were highly dependent on Zostera but were also present at the unvegetated sites. Only Fundulus heteroclitus and a few other rare species were collected solely in unvegetated habitats. All of the target species except P. americanus and O. mordax occurred more often in areas of vegetation or Microciona than in sandy areas. The attractiveness of Zostera over other habitats has been ascribed to characteristics of seagrass habitat (Bell & Pollard, 1989; Orth et al., 1984). Seagrass canopies provide shade, reduced water currents and increased surface area (Bell & Pollard, 1989) while the rhizome
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mat provided further habitat complexity (Orth et al., 1984). These attributes along with higher primary productivity provided an abundant and varied food supply as well as protection from predators. For example, the predation efficiency of cottids feeding on YOY G. morhua was inversely related to habitat complexity (Tupper & Boutilier, 1995a) and YOY G. morhua kept in aquaria selected more complex substrates in the presence of predators (Gotceitas & Brown, 1993). Thus the relationship between habitat complexity and population density can be attributed to differential predation among habitat types and need not be related to competition for living space. Growth rates of YOY G. morhua in St Margaret’s Bay were higher in seagrass beds than on rocky reef, cobble or sand bottoms (Tupper & Boutilier, 1995b) and were attributed to greater prey densities in seagrass habitat. Larger individuals were rare in our mid-coast coast samples and mainly restricted to presumed age 1+ juvenile P. americanus remaining from the previous year’s recruitment, or adults of species that breed in the immediate environment, such as G. aculeatus and M. aenaeus. Many recreationally and commercially important species such as Anguilla rostrata, Clupea harengus, Gadus morhua, Microgadus tomcod, Pollachius virens, Urophycis chuss, U. regia, U. tenuis, Osmerus mordax, Macrozoarces americanus, T. adspersus, and Pleuronectes americanus used shallow habitats in mid-coast coast Maine estuaries as indicated by the prevalence of their YOY and juveniles in our collections. A similar nursery function has often been observed in marsh systems and other shallow areas elsewhere in the north Atlantic Ocean (Ayvazian et al., 1992; Gibson, Ansell, & Robb, 1993; Heck et al., 1989; Kneib, 1997; Lazzari et al., 1999; Nixon & Oviatt, 1973; Pearcy & Richards, 1962; Sogard & Able, 1991; Weinstein, 1979). For over three decades, about 65% of the coastal fishery resources in the U.S. were thought to be estuarine dependent (McHugh, 1966). However, a revised estimate based on commercial fishery landings indicated that well over 75% by weight of commercially important fishes were dependent of estuaries for reproduction, nurseries, food production or migration (Chambers, 1992) with a much lower percentage (32%) considered estuarine dependent in the northwestern Atlantic Ocean. Heck et al. (1989) found a similar estimate of 34% (by number) of the fish species collected in Nauset Marsh, Cape Cod were either commercially or recreationally important. However, we collected a greater percentage (38%) of these fishes overall and the percentage approached 50% in both Casco Bay (44%) and the Weskeag River (46%). The importance of shallow habitats as nurseries has been demonstrated for species of recreational and commercial importance including G. morhua and P. virens in Canada (Keats, 1986; Keats, South, & Steele, 1987; MacDonald et al., 1984) and in
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Europe (Daan, 1978; Edwards & Steele, 1968; Gibson et al., 1993), but this was the first Maine study to do so. We found YOY G. morhua in all habitats of the three mid-coast estuaries sampled from April through June documenting the importance of these estuarine areas as nurseries on, at least, a seasonal basis. Three other gadoid species (M. tomcod, P. virens, and U. tenuis) of commercial or recreational importance also were common during the spring and YOY U. chuss, T. adspersus, and P. americanus were common components of the fish communities. The shallow habitats sampled in this study were undoubtedly important habitat for gadoids seasonally and for P. americanus almost year-round thus making these fishes susceptible to impacts from coastal pollution and habitat degradation putting the adult fisheries at risk by adversely affecting recruitment. A similar shallow water fish community was observed throughout the northwest Atlantic Ocean from the Canadian Maritimes to Virginia. We compared our results with other habitat studies using seining and trawling methods in Virginia (Orth & Heck, 1980), New Jersey (Szedlmayer & Able, 1996), New York (Briggs & O’Connor, 1971), Connecticut (Warfel & Merrimen, 1944), Rhode Island (Pearcy & Richards, 1962), Massachusetts (Heck et al., 1989), Maine (Ayvazian et al., 1992; Lazzari et al., 1999) and Atlantic Canada (Black & Miller, 1991; MacDonald et al., 1984; Tyler, 1971). As expected, the Maine fish fauna was similar to Massachusetts and intermediate in composition compared with Canada and more southern areas. The fish community in Maine shallow waters consisted primarily of cold temperate species and few of the southern species that add to the faunal richness of New Jersey and Virginia estuaries occurred here. The dominant Maine species of P. americanus, G. aculeatus, A. quadracus, and M. aenaeus had a wide geographic distribution despite important differences in the dominant marsh vegetation, tidal flood regimes, temperature range, and other factors. Seasonal differences in species richness and abundance occurred with peak numbers of species and CPUE occurring in warmer months between June and October in mid-coast coast Maine estuaries. Typically, in northern shallow marine habitats, the summer–autumn assemblage, consisting predominantly of juvenile and small adult fishes, moved from shallow water to offshore habitats in response to declining winter water temperatures (Lazzari et al., 1999; MacDonald et al., 1984; Tyler, 1971) leaving the remaining winter assemblage low in diversity and number and represented by only the most physiologically tolerant species. Seasonal movement from inshore habitat to offshore was important for individual species and resulted in seasonal changes in fish species composition and abundance such that summer–autumn was characterized by a community richer in individuals and species. Seasonal movement from inshore habitat to offshore was unidirectional for
the individual of many species, such as C. harengus and the gadoids, since the shallow water community consisted of a new 0+ yearclass each year. For other species (P. americanus, M. aenaeus), the return inshore was an annual occurrence, triggered by resource availability and predator avoidance (MacDonald et al., 1984). Seasonal movements have been commonly reported elsewhere (Creutzberg & Fonds, 1971; Horn, 1980; Ross, McMichael, & Ruple, 1987) with seasonal patterns within estuaries being attributed to shifts in faunal composition, immigration and emigration from estuaries, and predator–prey interactions (Haedrich, 1983; Nixon & Oviatt, 1973; Rountree & Able, 1992). Other factors contributing to the changes in species number and abundance over time were likely to be emigration into deeper water, as was known to take place in P. americanus (Pearcy, 1962) or a result of the increasing size of many species that made them less vulnerable to our sampling gear. Seasonal patterns in species richness and faunal abundance were observed in Canada (MacDonald et al., 1984; Tyler, 1971), Maine (Ayvazian et al., 1992; Lazzari et al., 1999; Recksiek & McCleave, 1973), Rhode Island (Nixon & Oviatt, 1973), and New Jersey (Rountree & Able, 1992), although the timing of peak species richness and abundance exhibited spatial and annual variation in a particular studies. In summary, fish species richness and faunal abundances were positively associated with vegetation, particularly Zostera ,in three mid-coast coast Maine estuaries. The fish community found in these estuaries was dominated by young-of-the-year and juveniles and all five of the habitats sampled function as nursery areas. A greater percentage of commercial and recreational species was collected in this study than in previous studies in estuaries from the northwest Atlantic Ocean. This study documents the importance of shallow estuarine areas in Maine as nurseries for many commercial and recreational species. Additional research will be needed to determine the relative importance of shallow habitats to the overall recruitment of these fishes. Acknowledgements We would like to thank M. Lucas and J. Lewis for field assistance. This project was funded by the WallopBreaux Trust Fund for Sportfish Restoration. References Adams, S. M. (1976). The ecology of eelgrass, Zostera marina (L.), fish communities. 1. Structural analysis. Journal of Experimental Marine Biology and Ecology 22, 269–291. Ayvazian, S. G., Deegan, L. A., & Finn, J. T. (1992). Comparison of habitat use by estuarine fish assemblages in the Acadian and Virginian zoogeographic provinces. Estuaries 15, 368–383.
M.A. Lazzari et al. / Estuarine, Coastal and Shelf Science 56 (2003) 73–84 Bell, J. D., & Pollard, D. A. (1989). Ecology of fish assemblages and fisheries associated with seagrasses. In A. W. D. Larkum, A. J. McComb, Shepard, & S. A., Shepard (Eds.), Biology of Seagrasses (pp. 565–609). Amsterdam: Elsevier. Bigelow, H. B., & Schroeder, W. C. (1953). Fishes of the Gulf of Maine. Fishery Bulletin 53, 1–477. Black, R., & Miller, R. J. (1991). Use of the intertidal zone by fish in Nova Scotia. Environmetal Biology of Fishes 31, 109–121. Briggs, P. T., & O’Connor, J. S. (1971). Comparison of shore-zone fishes over naturally-vegetated and sand-filled bottoms in Great South Bay. New York Fish and Game Journal 18, 25–41. Brown, A. C., & McLachlan, A. (1990). Ecology of Sandy Shores (328 pp.). Amsterdam: Elsevier. Chambers, J. R. (1992). Coastal degradation and fish population losses. In R. H. Stroud (Ed.). Stemming the Tide of Coastal Fish Habitat Loss. Marine recreational fish symposium. Proceedings of the National Symposium on Fish Habitat Conservation, Baltimore, MD (pp. 45–51). Creutzberg, F., & Fonds, M. (1971). The seasonal variation in the distribution of some demersal fish species in the Dutch Wadden Sea. Thalassia Jugoslovia 7, 13–23. Daan, N. (1978). Changes in cod stock and cod fisheries in the North Sea. In G. Hempel (Ed.). North sea fish stocks—recent changes and their causes. Rapports et Proces-Verbaux des Reunions conseil International pour l’Exploration de la Mer 172 (pp. 39–57). Edwards, R. R. C., & Steele, J. H. (1968). The ecology of 0+ group plaice and common dabs at Loch Ewe. 1. Population and food. Journal of Experimental Marine Biology and Ecology 2, 215–238. Field, J. G., Clarke, K. R., & Warwick, R. M. (1982). A practical strategy for analyzing multispecies distribution patterns. Marine Ecology Progress Series 8, 37–52. Gibson, R. N., Ansell, A. D., & Robb, L. (1993). Seasonal and annual changes in the abundance and species composition of fish and marcocrustacean communities on a Scottish sandy beach. Marine Ecology Progress Series 98, 89–105. Gotceitas, V., & Brown, J. A. (1993). Substrate selection by juvenile Atlantic cod (Gadus morhua): effects of predation risk. Oecologia 93, 31–37. Haedrich, R. L. (1983). Estuarine fishes. In B. H. Ketchum (Ed.), Ecosystems of the world (pp. 183–207). Amsterdam: Elsevier. Heck, K. L., Jr., Able, K. W., Fahay, M. P., & Roman, C. T. (1989). Fishes and decapod crustaceans of Cape Cod eeelgrass meadows, species composition, seasonal abundance patterns and comparison with unvegetated substrates. Estuaries 12, 59–65. Heck, K. L., Jr., & Thoman, T. A. (1981). Experiments on predator– prey interactions in vegetated aquatic habitats. Journal of Experimental Marine Biology and Ecology 53, 125–134. Heck, K. L., Jr., & Thoman, T. A. (1984). The nursery role of seagrass meadows in the upper and lower reaches of the Chesapeake Bay. Estuaries 7, 70–92. Heck, K. L., Jr., & Wilson, K. A. (1987). Predation rates on decapod crustaceans in latitudinally separate seagrass communities, a study of spatial and temporal variation using tethering techniques. Journal of Experimental Marine Biology and Ecology 107, 87–100. Horn, M. H. (1980). Diel and seasonal variation in abundance and diversity of shallow water fish populations in Morro Bay, California. Fishery Bulletin 78, 759–770. Huh, S. H. (1984). Seasonal variations in populations of small fishes concentrated in shoalgrass and turtle grass meadows. Journal of the Oceanological Society of Korea 19, 44–55. Keats, D. W. (1986). A method for the underwater quantification of juvenile cod abundance. Canadian Journal of Aquatic Fishery Science Research Document 185, 1–53. Keats, D. W., South, G. R., & Steele, D. H. (1987). The role of macroalgae in the distribution and feeding of juvenile codfish (Gadus morhua) L. in inshore waters off eastern Newfoundland. Canadian Journal of Zoology 65, 49–53.
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Kneib, R. T. (1987). Predation risk and use of intertidal habitats by young fishes and shrimp. Ecology 67, 379–386. Kneib, R. T. (1997). The role of tidal marshes in the ecology of estuarine nekton. Oceanography and Marine Biology: An Annual Review 35, 163–220. Lazzari, M. A., Sherman, S., Brown, C. S., King, J., Joule, B. J., Chenoweth, S. B., & Langton, R. W. (1999). Seasonal and annual variations in abundance and species composition of nearshore fish communities in Maine. Estuaries 22, 636–647. Lazzari, M. A., & Tupper, B. (2002). Importance of shallow water habitats for demersal fishes and decapod crustaceans in Penobscot Bay, Maine. Environmental Biology of Fishes 63, 57–66. Leber, K. M. (1985). The influence of predatory decapods, refuge, and microhabitat selection on seagrass communities. Ecology 66, 1951– 1964. MacDonald, J. S., Dadswell, M. J., Appy, R. G., Melvin, G. D., & Methven, D. A. (1984). Fishes, fish assemblages and their seasonal movements in the lower Bay of Fundy and Passamaquoddy Bay, Canada. Fishery Bulletin 82, 121–139. McHugh, J. L. (1966). Management of estuarine fishes. American Fisheries Society Special Publication 3, 133–154. Nixon, S. W., & Oviatt, C. (1973). Ecology of New England salt marsh. Ecological Monographs 43, 463–498. Orth, R. J., & Heck, K. L., Jr. (1980). Structural components of eelgrass (Zostera marina) meadows in the lower Chesepeake Bay—Fishes. Estuaries 3, 278–288. Orth, R. J., Heck, K. L., Jr., & van Montfrans, J. (1984). Faunal communities in seagrass beds, a review of the influence of plant structure and prey characteristics on predator–prey relationships. Estuaries 7, 339–350. Orth, R. J., & van Montfrans, J. (1987). Utilization of seagrass meadows and tidal marsh creek by blue crabs Callinectes sapidus. 1. Seasonal and annual variations in abundance with emphasis on post-settlement juveniles. Marine Ecology Progress Series 41, 283– 294. Paterson, A. W., & Whitfield, A. K. (2000). The ichthyofauna associated with an intertidal creek and adjacent eelgrass beds in the Kariega estuary, South Africa. Environmental Biology of Fishes 58, 145–156. Pearcy, W. G. (1962). The ecology of an estuarine population of winter flounder, Psuedopleuronectes americanus (Walbaum), III. Bulletin Bingham Oceanographic Collection 18, 39–64. Pearcy, W. G., & Richards, S. W. (1962). Distribution and ecology of fishes of the Mystic River, Connecticut. Ecology 43, 248–259. Recksiek, C. W., & McCleave, J. D. (1973). Distribution of pelagic fishes in the Sheepscot River—Back River estuary, Wiscasset, Maine. Transactions of the American Fisheries Society 102, 541– 551. Ross, S. T., McMichael, R. H., Jr., & Ruple, D. L. (1987). Seasonal and diel variation in the standing crop of fishes and macroinvertebrates from a Gulf of Mexico surf zone. Estuarine, Coastal and Shelf Science 25, 39–141. Rountree, R. A., & Able, K. W. (1992). Faunal composition of marsh creeks in New Jersey. Estuaries 15, 171–185. Sogard, S. M., & Able, K. W. (1991). A comparison of eelgrass, sea lettuce macroalgae, and marsh creeks as habitat for epibenthic fishes and decapod crustaceans. Estuarine, Coastal and Shelf Science 33, 501–520. Sogard, S. M., Powell, G. V. N., & Holmquist, J. G. (1987). Utilization by fishes of shallow seagrass-covered banks in Florida Bay, 2. Diel and tidal patterns. Environmental Biology of Fishes 24, 81–92. Sokal, R. R., & Rohlf, F. J. (1981). Biometry, 2nd ed. (pp. 859). New York: W.H. Freeman. Stoner, A. W. (1982). The influence of benthic macrophytes on the foraging behavior of the pinfish, Lagodon rhomboides (Linnaeus). Journal of Experimental Marine Biology and Ecology 58, 271–284.
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Nursery use of shallow habitats by epibenthic fishes in Maine nearshore waters M.A. Lazzari*, S. Sherman, J.K. Kanwit Maine Department of Marine Resources, P.O. Box 8, West Boothbay Harbor, ME 04575, USA Received 4 June 2001; received in revised form 10 December 2001; accepted 10 December 2001
Abstract Species richness and abundance of epibenthic fishes were quantified with daytime beam trawl tows in shallow water habitats during April–November 2000 of three mid-coast Maine estuaries; Casco Bay, Muscongus Bay and the Weskeag River. Five shallow (<10 m) habitats were sampled, Zostera marina, Laminaria longicruris, Phyllophora sp., Microciona prolifera and unvegetated sandy areas. Thirty-two species of fishes were collected. Species richness tow1 was greater in Casco Bay followed by the Weskeag River and Muscongus Bay respectively. Catch per unit effort (CPUE) of fishes was greater in Casco Bay than in the Weskeag River or Muscongus Bay. Species richness and faunal abundances were positively associated with vegetation, particularly Zostera, at all sampling locations. CPUEs of fishes were higher in Zostera due primarily to the abundance of Gasterosteus aculeatus, Apeltes quadracus, Pungitius pungitius, Myoxocephalus aenaeus, and Cylcopterus lumpus. The fish community of mid-coast estuaries was dominated by young-of-the-year (YOY) and juvenile fishes and all of the habitat types function as nursery areas. Twelve species (38%) of commercial and recreational importance were collected in the three estuaries, but the percentage was higher in Casco Bay (44%) and the Weskeag River (46%). These species included Anguilla rostrata, Clupea harengus, Gadus morhua, Microgadus tomcod, Pollachius virens, Urophycis chuss, Urophycis regia, Urophycis tenuis, Osmerus mordax, Macrozoarces americanus, Tautogolabrus adspersus, and Pleuronectes americanus. Four species, G. morhua, M. tomcod, P. virens, and U. tenuis were more common in spring than summer or autumn. Pleuronectes americanus was most abundant in summer followed by spring and autumn respectively. This study documents the importance of shallow estuarine areas in Maine as nurseries for these species. 2003 Elsevier Science B.V. All rights reserved. Keywords: Zostera; Community composition; Maine coast; Estuarine fauna
1. Introduction The fish fauna of the deeper areas of the Gulf of Maine (GOM) system was well described (Bigelow & Schroeder, 1953), and published studies on shallow water fish communities in the region exist for Passamaquoddy Bay (MacDonald, Dadswell, Appy, Melvin, & Methven, 1984; Tyler, 1971), Penobscot Bay (Lazzari & Tupper, 2002), the Sheepscot River (Recksiek & McCleave, 1973), Montsweag Bay (Targett & McCleave, 1974), Sagadahoc Bay (Lazzari et al., 1999) and Wells Harbor (Ayvazian, Deegan, & Finn, 1992). The majority of these fish
* Corresponding author. E-mail address: [email protected] (M.A. Lazzari).
community studies were relatively short term (Ayvazian et al., 1992; Recksiek & McCleave, 1973; Targett & McCleave, 1974; Tyler, 1971), often lasting a year or less. Many were close to 30 years old and provide little information on the basic ecology of recreational and commercial finfish species. Recent impacts of intensive human development of the shore-line and increased exploitation of the fisheries stocks on species composition, abundance and habitat use by many recreationally and commercially important species were unknown. In order to effectively manage marine recreational and commercial finfish species such as Pleuronectes americanus, Gadus morhua, and Pollachius virens, information was needed on the distribution, abundance, and habitat requirements of the juvenile stages of these species in shallow habitats. The 1996 amendments to the
0272-7714/03/$ - see front matter 2003 Elsevier Science B.V. All rights reserved. doi:10.1016/S0272-7714(02)00122-1
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Magnuson–Stevens Fishery Conservation and Management Act, known as the Sustainable Fisheries Act (SFA), emphasized the importance of habitat protection to healthy fisheries and strengthened the ability of the National Marine Fisheries Service (NMFS) and the regional fishery management councils to protect and conserve essential marine, estuarine, and anadromous fish habitat. Information on the nearshore distribution of epibenthic fishes was important due to the nursery function of shallow inshore habitats, the environmental variability of these areas, and the high potential for anthropogenic impact (Brown & McLachlan, 1990; Kneib, 1997; MacDonald et al., 1984; Warfel & Merrimen, 1944). The importance of vegetation, particularly Zostera marina and other seagrasses as epibenthic fish habitat has been demonstrated outside the GOM (Heck, Able, Fahay, & Roman, 1989; Huh, 1984; Paterson & Whitfield, 2000; Sogard & Able, 1991; Sogard, Powell, & Holmquist, 1987; Szedlmayer & Able, 1996; Weinstein & Brooks, 1983) with higher faunal densities found in seagrass relative to unvegetated sand or mud substrates (see review in Orth, Heck, & van Montfrans, 1984). Seagrass functions as nursery habitat for newly settled juvenile fishes and decapods (Adams, 1976; Bell & Pollard, 1989; Heck et al., 1989; Heck & Thoman, 1984; Orth & van Montfrans, 1987) and has a demonstrated value as a refuge from predation (Heck & Thoman, 1981; Heck & Wilson, 1987; Kneib, 1987; Leber, 1985; Paterson & Whitfield, 2000; Stoner, 1982; Wilson, Heck, & Able, 1987). However, many studies have been restricted to a single habitat and very few compared ichthyofaunal utilization of different habitats within the same estuary. The purpose of this study was to determine the species composition and relative abundance of epibenthic fishes, particularly juvenile forms of marine recreational and commercial species (Gadus morhua, Microgadus tomcod, Pollachius virens, Urophycis chuss, U. tenuis, Osmerus mordax, Tautogolabrus adspersus, and Pleuronectes americanus) and their habitats in the shallow (<10 m) waters of mid coastal Maine estuaries by (1) documenting their seasonal presence and relative abundance and (2) relating their occurrence to habitat through beam trawl sampling.
2. Materials and methods 2.1. Study area Three estuaries with Zostera marina (eelgrass) present and located in mid coastal Maine (Casco Bay, Muscongus Bay, Weskeag River) were sampled in this study (Fig. 1). The Cousins Island area of Casco Bay (7015¢, 4378¢) was characterized by low relief, moderate
Spartina alterniflora salt marsh, expansive areas of Zostera and adjacent mudflat and mussel areas. Freshwater input from the Royal River was moderate though surface salinities were high (>25 PSU) with the exception of station 1 following rainfall. Tides were semidiurnal and in the 2.4–3.2 m range. The Muscongus Bay estuary (longitude 6940¢, latitude 4395¢) was characterized by moderate relief, minimal saltmarsh and large areas of mudflat. Freshwater input from the Medomak River was low and salinities were high. Tides were semidiurnal and range from 2.5–3.3 m and discrete areas of submerged aquatic vegetation (Zostera, Laminaria longicruris, kelp and Phyllophora sp., algae) were present. The Weskeag River estuary (6920¢, 4398¢) was distinguished by moderate relief, nominal salt marsh but expansive mudflat and mussel areas. Freshwater input was minimal and salinities were always high. Tides were semidiurnal and ranged from about 2.5–3.5 m and large areas of aquatic vegetation (Zostera and Laminaria) were present. 2.2. Field methods Sampling for juvenile fishes in shallow subtidal habitats in mid-coast coast estuaries began in early April and continued into November 2000. Ten stations with towable bottom were selected and sampled bimonthly during daylight hours in Muscongus Bay and the Weskeag River and 11 stations were sampled in Casco Bay. All stations sampled were between one and 10 m in depth. At each station, one 5 min tow was made with a small beam trawl (2.0 · 0.5 m opening, 3 mm codend mesh). Samples were sorted live and discarded except for species of particular interest which were preserved in 10% formalin. All fishes were identified, counted and measured for total length (cm). Surface temperature and salinity by refractometry were recorded at each site and depth was measured using a hull mounted electronic depth finder. 2.3. Statistical analyses Fish catches were expressed as number tow1 (CPUE) for the beam trawl samples. All statistical testing used SYSTAT statistical software (Wilkinson, 1996). Our primary objective was to identify patterns of species associations in several habitats. The method traditionally used in fish-community studies to identify groups of species or stations has been cluster analysis, usually using an agglomerative clustering algorithm. This method produces a classification diagram (dendrogram), which also shows the hierarchical relationships between groups. Patterns of occurrence were tested using cluster analysis (CA) and multidimensional scaling (MDS, Field, Clarke, & Warwick, 1982). In each
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Fig. 1. Station locations in mid-coast Maine estuaries (Casco Bay, Muscongus Bay and the Weskeag River) sampled with beam trawl from April through November 2000.
analysis, samples taken at each station were combined and rare fish species (3 individuals caught during the entire study) were excluded. The among station similarity matrix was computed using CPUE data that were root–root transformed in order to reduce the influence of the most abundant species and association matrices were produced using Bray–Curtis similarity measures. CA were prepared for each estuary separately while MDS was performed with all stations combined. Secondly, to compare species number tow1 and CPUE of the fishes across the various estuaries and habitats, one-way analyses of variance (ANOVA) testing followed by a priori SD (least significant difference) (LSD) multiple comparisons tests or two-sample t-tests were used when the data met the assumptions of normality and heterogeneity of variance, following the method of means testing outlined by Sokal and Rohlf (1981). Species richness and CPUEs (including all sampling dates) were compared for the three estuaries using ANOVA for unbalanced designs. Additional ANOVAs (unbalanced designs) of species richness and CPUE were run for three depth ranges (0–3 m, 3–6 m, 6–10 m) and for three seasons [spring (April–June),
summer (July–September), and autumn (October–November)]. All numbers were log10 transformed prior to analysis. Although concerns for experimental error rate exist when multiple comparisons were made in a given study, the objective of this study was to make a series of individual comparisons. Due to the robustness of ANOVA and the highly significant differences among groups (P < 0:001 for the overall ANOVA for most tests), the results of the ANOVA’s and planned comparisons could be interpreted reliably. Two-sample t-tests for unequal variances (Sokal & Rohlf, 1981) were used to determine whether means of species richness and CPUE of all species differed between Zostera and unvegetated sandy habitats in each estuary. Two-sample t-tests for unequal variances (Sokal & Rohlf, 1981) were also used to determine whether means of CPUE of individual species differed between Zostera and unvegetated sandy habitats. These comparisons were designed to determine the relative value (in terms of mean species richness or CPUE) of the different habitats for the common epibenthic fishes and the eight target species. These multiple comparisons provided a general view of habitat relationships since it was not possible to directly
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compare each habitat without there being some influence of site location within the estuary because the same substrate types did not occur at all sites.
3. Results 3.1. Site characteristics Surface salinities differed little among sites in the Weskeag River and Muscongus Bay ranging from 28 to 33 PSU from April through November while salinities in Casco Bay were more variable, ranging from 22 to 31 PSU. On average, the maximum difference in salinity across all sites within an estuary was <5 PSU with the only exception being Casco Bay station 1 (18 PSU). Surface water temperatures were similar among the three estuaries with slightly warmer water (1–2 C) occurring in Casco Bay. Water temperatures everywhere increased from a minimum of 6 C in April to a maximum of 17 C in late July before dropping gradually during the autumn. By November, temperatures averaged about 9 C. Little variation was
observed in water temperatures among stations within each estuary during any sampling period (<2 C). Vegetation was a widespread habitat component in Casco Bay and in the Weskeag River relative to Muscongus Bay. Zostera marina (eelgrass) occurred at four stations in Casco Bay and the Weskeag River, but only at two stations in Muscongus Bay. Laminaria longicruris (kelp) occurred at one station in the Weskeag River and occasionally in Casco and Muscongus Bays as did Phyllophora sp. (algae) in Muscongus Bay. Microciona prolifera (sponge) occurred consistently at one station sampled in Casco Bay. A total of 416 beam trawl tows were collected in Casco Bay (n ¼ 147), Muscongus Bay (139) and the Weskeag River (130) (Table 1). Depending on the weather, the number of stations sampled on a sampling trip varied from 6–12 in Casco Bay, 6–13 in Muscongus Bay and 4–11 in the Weskeag River. The fewest number of tows were made in April (16) while the highest number were collected in late July and early August (34). By habitat, more tows were made on sandy substrate (236) than were made in areas vegetated with Zostera (134), Laminaria (34), in Microciona (10) or
Table 1 Sampling effort, species richness (total and mean SE species per tow), and CPUE (mean SE number per tow) for stations in Casco Bay, Montsweag Bay and the Weskeag River, Maine. Vegetation (veg.) Psp ¼ Phyllophora sp.; Zm ¼ Zostera marina; Ll ¼ Laminaria longicruris; Mp ¼ Microciona prolifera Estuary
Station (veg.)
Number of tows
Total species
Mean species per tow
Mean CPUE
Casco Bay
1 2 3 4 5 6 7 8 9 10 11
(Zm) (Mp)
13 13 14 13 14 14 14 12 13 14 11
13 11 18 17 18 16 17 9 10 19 12
3.7 0.5 2.9 0.4 4.3 0.7 6.2 0.7 6.1 0.6 3.0 0.5 4.0 0.6 2.4 0.3 2.9 0.4 6.9 0.5 3.1 0.5
10.6 3.1 9.4 2.6 13.5 2.7 66.9 16.5 48.9 10.0 9.3 2.4 16.6 6.1 6.7 1.9 10.0 2.3 74.7 19.9 9.1 2.5
Montsweag Bay
1 (Zm) 2 3 4 (Psp) 5 6 7 (Zm) 8 9 10
13 12 14 12 13 13 13 13 11 11
13 10 10 14 11 9 13 9 15 9
4.0 0.5 3.2 0.5 2.4 0.3 3.5 0.5 2.2 0.4 2.7 0.4 4.9 0.5 2.2 0.3 3.5 0.5 2.4 0.4
34.9 18.2 11.4 2.6 6.8 1.3 14.9 4.8 6.7 0.9 3.3 0.6 22.3 3.9 12.6 2.6 12.6 3.4 5.6 1.9
Weskeag River
1 2 3 4 5 6 7 8 9 10
14 13 14 14 13 11 14 13 11 10
10 7 13 17 11 9 15 13 15 3
2.4 0.4 1.9 0.3 3.5 0.4 4.1 0.5 2.8 0.2 2.1 0.3 5.5 0.8 4.2 0.6 5.6 0.4 1.5 0.2
4.1 1.2 4.9 1.4 6.4 1.7 10.4 2.9 6.7 1.0 7.0 1.9 27.3 11.3 85.1 26.7 41.2 13.1 2.5 0.5
(Zm) (Zm) (Zm)
(Ll) (Zm)
(Zm) (Zm) (Zm)
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Phyllophora (2) (Table 1). In all three estuaries, more tows were made in sandy than in vegetated areas.
richness and abundance were greatest at the stations where Zostera was present regardless of estuary.
3.2. Species richness
3.3. Habitat selection
A total of 32 species were collected in the three estuaries with a similar number in each estuary, 25 species in Casco Bay, 24 in Muscongus Bay and 22 in the Weskeag River. However, overall species tow1 was significantly greater in Casco Bay followed by the Weskeag River and Muscongus Bay respectively (ANOVA, F2;413 ¼ 19:2, P< 0.001). The fish fauna was dominated by a relatively few species, but the temporal and habitat patterns of species richness varied. Apeltes quadracus (fourspine stickleback), Pungitius pungitius (ninespine stickleback), Myoxocephalus aenaeus (grubby), Gasterosteus aculeatus (threespine stickleback), and Pleuronectes americanus (winter flounder), made up 73% of the total fishes collected. Twelve commercial and recreational species, including six gadoid species were collected. These included Anguilla rostrata (American eel), Clupea harengus (Atlantic herring), Gadus morhua (cod), Urophycis tenuis (white hake), U. regia (spotted hake), U. chuss (red hake), Pollachius virens (pollock), Microgadus tomcod (tomcod), Tautogolabrus adspersus (cunner), Macrozoarces americanus (ocean pout), Osmerus mordax (rainbow smelt) and Pleuronectes americanus (winter flounder). Seventeen species occurred in all three estuaries including eight commercial and recreational species. Five species were represented by a single individual including Fundulus heteroclitus (mummichog), Ulvaria subbifurcata (radiated shanny), Myoxocephalus scorpius (shorthorn sculpin), M. octodecimspinosus (longhorn sculpin) and Dactylopterus volitans (flying gurnard). Two of the most abundant species (M. aenaeus and P. americanus) were widely distributed in the three estuaries (Table 2). Myoxocephalus aenaeus and P. americanus occurred in more tows (>50%) than any other species. Syngnathus fuscus (northern pipefish), Pholis gunnellus (rock gunnel) and Cyclopterus lumpus (lumpfish) all occurred in greater than 20% of the tows. G. morhua, U. tenuis, U. chuss, P. virens, M. tomcod, and T. adspersus occurred in 9–14% of tows while O. mordax were in 5%. Six species (G. morhua, U. tenuis, T. adspersus, P. gunnellus, M. aenaeus, P. americanus) occurred in all five habitats sampled (Table 2); five other species occurred in all habitats except Phyllophora. Seven species occurred in a single habitat, usually sand. Clupea harengus, M. tomcod, U. regia, and M. americanus were not present in all estuaries. The total number of species was highest on sand (29) followed by Zostera (26), Laminaria (16), Microciona (13), and Phyllophora (10). The high species number observed in unvegetated sandy areas was due to increased sampling effort that resulted in the collection of uncommon species such as the Myoxocephalus species. However, mean fish species
Species richness by station (Fig. 2a) was generally highest in Zostera in Casco Bay (stations 4, 5, 10), Muscongus Bay (stations 1, 7) and the Weskeag River stations (4, 7, 8, 9). However, station 7 in Zostera in Casco Bay was an exception. More species generally occurred at stations 4 and 9 in Muscongus Bay where Phyllophora or Laminaria was sometimes encountered and in the Weskeag River where Laminaria (station 3) occurred. CPUE (Fig. 2b) followed the same pattern, being highest at stations with Zostera in all three estuaries. The results of cluster analyses (CA) classified the Casco Bay, Muscongus Bay and Weskeag River stations into habitat groups based on species richness (Fig. 3). A major dichotomy classified three stations (4, 5, 10) in Casco Bay (Fig. 3a) located in shallow Zostera and possessing the greatest species diversity from the eight remaining stations with fewer species present. Two other stations, one in a channel area (3) and another in sparse Zostera (7) were joined next to last. The deepest site (station 8) in Casco Bay had low CPUE and species diversity. Similar trends were revealed in the cluster analyses of stations in Muscongus Bay (Fig. 3b) and the Weskeag River (Fig. 3c). The deepest station in Muscongus Bay (6) and in the Weskeag River (10) also had low diversity and CPUE and were the last stations added to their respective dendrograms. The two stations with Zostera (1, 7) in Muscongus Bay were the next least similar to the other sites, followed by station 9 where Zostera was present in two tows. In the Weskeag River (Fig. 3c). three shallow stations with Zostera (7, 8, 9) were joined next to last, preceded by another station where Zostera occurred, station 4. Non-metric multidimensional scaling analysis (MDS) of the mid coast fish data also grouped individual stations based on habitat and species number similar to the cluster analysis results (Fig. 4). The shallow stations with Zostera in Casco Bay (4, 5, 10), in Muscongus Bay (1, 7) and in the Weskeag River (4, 7, 8, 9) were grouped together. However, one station in sparse Zostera in Casco Bay (station 7) was placed into the larger grouping of stations located primarily on sandy substrates. Six of the remaining stations with low species richness formed a grouping bounded by the stations in deepest water in each estuary (c8, m6, w10). In summary, the two multivariate methods generally grouped stations with Zostera together. 3.4. Abundance A total of 7300 fishes (32 species) were collected with the beam trawl. Total abundance was greater in Casco
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Table 2 Fishes (n ¼ 32 species), CPUE (number tow1) and percent frequency of occurrence collected in shallow habitats in mid-coast Maine estuaries with 2.0 m beam trawl from April to November 2000. Estuaries are Casco Bay (CB), Muscongus Bay (MB), Weskeag River (WR). Habitats are Phyllophora sp. (Psp), Zostera marina (Zm), Laminaria longicruris (Ll), Microciona prolifera (Mp) and sand (S); p ¼ present Estuary
Habitat
Family species effort
Common name
CB 147
MB 139
WR 130
Psp 2
Zm 134
Ll 34
Mp 10
Sand 236
Anguilla rostrata
American eel
Clupea harengus
Atlantic herring
Osmerus mordax
Rainbow smelt Atlantic cod
Microgadus tomcod
Atlantic tomcod
Pollachius virens
Pollock
Urophycis chuss
Red hake
Urophycis regia
Spotted hake
Urophycis tenuis
White hake
Macrozoarces americanus
Ocean pout
Fundulus heteroclitus
Mummichog
Menidia menidia
Atlantic silverside
Apeltes quadracus
Fourspine stickleback
Gasterosteus aculeatus
Threespine stickleback
Gasterosteus wheatlandi
Blackspotted stickleback
Pungitius pungitius
Ninespine stickleback
Syngnathus fuscus
Northern pipefish
Tautogolabrus adspersus
Cunner
Lumpenus maculates
Daubed shanny
Ulvaria subbifurcata
Radiated shanny
Pholis gunnellus
Rock gunnel
Hemitriperus americanus
Sea raven
Myoxocephalus aenaeus
Grubby
M. octodecimspinosus
Longhorn sculpin
M. scorpius
Shorthorn sculpin
Cylcopterus lumpus
Lumpfish
Liparis atlanticus
Seasnail
Liparis coheni
Gulf seasnail
L. liparis
Striped seasnail
Dactylopterus volitans
Flying gurnard
<0.1 1 — — 0.1 2 0.3 9 — — 0.3 9 0.2 14 — — 0.3 10 <0.1 1 — — — — 3.1 8 0.2 7 — — <0.1 1 0.3 19 0.3 18 <0.1 1 <0.1 1 0.5 28 <0.1 1 3.1 54 <0.1 1 <0.1 1 0.2 9 — — — — <0.1 1 <0.1
<0.1 1 — — <0.1 1 0.4 11 0.3 12 0.3 13 0.4 16 0.1 5 0.6 25 — — — — — — <0.1 1 1.7 15 — — 8.4 22 0.2 12 0.1 9 — — — — 0.3 22 0.1 4 1.4 44 — — — — 1.1 36 <0.1 1 <0.1 2 <0.1 1 —
— — — — — — 4.0 p — — 1.5 p — — — — 3.0 p 1.0 p — — — — — — — — — — — — — — 0.5 p — — — — 1.5 p 0.5 p 27.5 p — — — — — — — — — — — — —
<0.1 1 <0.1 2 0.2 9 0.4 10 0.9 23 1.1 25 0.2 13 <0.1 3 0.5 19 <0.1 1 — — <0.1 3 13.8 41 6.1 53 <0.1 2 8.7 35 1.1 36 0.6 23 <0.1 1 — — 0.4 25 0.2 7 4.0 77 — — — — 1.2 44 <0.1 1 <0.1 1 — — —
— — — — — —
Gadus morhua
<0.1 1 <0.1 2 0.4 12 0.1 6 0.7 17 0.5 12 0.1 8 — — 0.1 8 <0.1 2 <0.1 1 <0.1 3 10.1 46 4.0 34 <0.1 3 0.7 16 1.2 42 0.4 14 <0.1 1 — — 0.2 14 0.2 8 2.2 57 — — — — 0.5 18 <0.1 1 — — — — —
— — — — 0.4 p 0.4 p — — — — 0.7 p — — 0.1 p — — — — — — 0.5 p — — — — — — 0.5 p 0.5 p — — — — 0.2 p 0.1 p 0.9 p — — — — 0.1 p — — — — — — —
<0.1 <1 — — 0.2 4 0.1 6 0.1 4 0.1 3 0.2 9 <0.1 1 0.2 9 <0.1 <1 <0.1 <1 <0.1 <1 0.3 9 <0.1 3 <0.1 <1 <0.1 3 0.4 21 0.1 8 <0.1 1 — — 0.3 17 <0.1 3 1.2 36 <0.1 <1 <0.1 <1 <0.1 7 — — <0.1 <1 <0.1 <1 <0.1
0.5 21 <0.1 3 0.3 15 0.4 26 — — 0.5 24 — — — — — — 0.1 6 — — — — <0.1 3 0.1 15 0.1 12 — — <0.1 3 0.5 35 — — 1.8 56 — — — — 1.0 29 <0.1 3 — — — — —
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M.A. Lazzari et al. / Estuarine, Coastal and Shelf Science 56 (2003) 73–84 Table 2 (continued ) Estuary Family species effort
Common name
Scopthalmus aquosus
Windowpane
Pleuronectes americanus
Winter flounder
Total species
CB 147 — 0.2 8 2.5 63 25
Habitat MB 139 1 0.1 6 1.9 46 24
Bay (n ¼ 3576) and the Weskeag River (2159) than in Muscongus Bay (1565). Dominant fishes were similar among estuaries with mean CPUE of A. quadracus, P. pungitius, M. aenaeus, G. aculeatus, and P. americanus about 2–5 individuals tow1 (Table 2). Apeltes quadracus, G. aculeatus, P. americanus and M. aenaeus comprising about 67% of the fishes collected in Casco Bay and A. quadracus, M. aenaeus, and P. americanus comprised about 70% of the fishes were collected in Muscongus Bay. In the Weskeag River, P. pungitius replaced A. quadracus as a dominant species and with G. aculeatus, P. americanus and C. lumpus made up about 80% of the fish abundance collected there. CPUE for all species was significantly greater (ANOVA, F2;413 ¼ 8:2, P < 0.001) in Casco Bay (24.3) compared with either the Weskeag River (16.6) or Muscongus Bay (11.3). Differences in CPUE existed by habitat within each system (Table 2). Fish CPUEs in Zostera within Casco Bay and the Weskeag River were about 12 times higher than in nearby unvegetated areas. In Casco Bay, most target species were more abundant in Zostera while in the other three habitats, P. americanus and O. mordax were more common. All of the target species in the Weskeag River were more abundant in Zostera although U. tenuis was common in Laminaria as well. Fish CPUE
Fig. 2. Mean number of fish species tow1 (a) and Catch per unit effort (number tow1) (b) of fishes collected by station with 2.0 m beam trawl in Casco Bay (CB), Muscongus Bay (MB) and the Weskeag River (WR) from April through November 2000. (*¼ Zostera present, ¼ uncommon habitat, see Table 1). r CB; h MB; M WR.
WR 130
Psp 2
Zm 134
Ll 34
Mp 10
Sand 236
— <0.1 1 1.2
— — — 1.5
— <0.1 1 1.6
— <0.1 3 1.6
— 1.4 p 3.1
<1 0.1 6 2.0
55 26
44 16
39 22
p 10
p 13
46 29
was six times higher in Zostera in Muscongus Bay but was greatest in the two tows made in Phyllophora. Of the target species collected in Muscongus Bay, P. virens, U. tenuis and T. adspersus were more abundant in Zostera and Phyllophora while U. chuss was more abundant in sandy areas. Gadus morhua and P. americanus were about equally abundant among the four habitats sampled. Fish CPUEs in Laminaria and Microciona within Casco Bay and in Laminaria within the Weskeag River, were also higher than tows in nearby unvegetated areas. Most of the fish species collected in this study were represented by young-of-the-year (YOY) and juveniles with the exception of winter flounder. Length frequencies of the eight common recreational and commercial species revealed all total lengths (TL) of G. morhua (mean=5.0, SD=0.5) and T. adspersus were less than 10 cm (4.4, 0.3). Five other species never exceeded 19 cm TL, including P. virens (mean=5.0, SD=0.4), O. mordax (6.3, 0.5), M. tomcod (7.4, 0.3), U. tenuis (8.3, 0.6), and U. chuss (9.3, 0.6); Pleuronectes americanus ranged from 1–42 cm TL, with most (63%) between 2 and 10 cm and a second group occurred at 12–16 cm (20%). Eleven P. americanus were greater than 20 cm. 3.5. Habitat comparisons Fish species richness tow1 and CPUE were higher for Zostera versus unvegetated sandy habitat. Overall species richness tow1 was positively associated with Zostera (two sample t-test, t ¼ 12:7, P < 0:001) as was total CPUE (two sample t-test, t ¼ 6:7, P < 0:001). Within all estuaries, greater species diversity and CPUE also occurred in Zostera relative to unvegetated areas (all two sample t-tests, t > 3:3, P < 0:001 except for CPUE in Muscongus Bay where t ¼ 2:4, P < 0:05). In individual species testing, CPUE of eight fishes (G. morhua, M. tomcod, G. aculeatus, A. quadracus, P. pungitius, C. lumpus, H. americanus, M. aenaeus) were significantly higher in tows in Zostera (all two sample t-tests, t > 2:0, P < 0:05) than unvegetated tows. CPUE of P. americanus was higher over sand (two sample t-test, t ¼ 2:2, P < 0:05). Percent total CPUE of the eight common target species ranged from 22 to 87% in Zostera and four species (U. tenuis, G. morhua, U. chuss, P. americanus)
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Fig. 4. Multidimensional scaling (MDS) of the fish samples caught by station with beam trawl in mid coast Maine estuaries from April through November 2000. The Casco Bay stations (c) were numbered 1–11 and stations in Muscongus Bay (m) and the Weskeag River (w) were numbered 1–10. (Zostera present at underlined stations, * ¼ uncommon habitats).
Fig. 3. Cluster analysis dendrograms of the fish samples collected by station with beam trawl in Casco Bay (a), Muscongus Bay (b) and the Weskeag River (c) from April to November 2000. (Zostera present at underlined stations, * ¼ uncommon habitats.)
also were common (>25%) in Laminaria. Osmersus mordax, U. chuss, T. adspersus, P. americanus, and G. morhua were common in the two rare habitats (Phyllophora sp. and Microciona) while on sandy habitats, P. americanus and O. mordax were common. 3.6. Seasonal and depth differences Species richness and CPUE showed peaks in late June/July and in September/October in the three estuaries. However, analyses of the mean number of
species tow1 for season for each estuary revealed that there were significantly more species of fishes present in spring (April–June) than in autumn (October–November) only in Casco Bay (ANOVA, F2;144 ¼ 3:03, P < 0:05). Species number was similar among seasons in Muscongus Bay and the Weskeag River. Similar analyses of mean CPUE of fishes for season in each estuary revealed that were there significantly more fishes present in summer (July–September) than in autumn (October–November) only in the Weskeag River (ANOVA, F2;127 ¼ 4:71, P < 0:01) with similar CPUEs among seasons in Casco and Muscongus Bays. The occurrence of several target species was seasonal with four gadoid species collected primarily in spring (April–June). Gadus morhua (two sample t-test, t ¼ 3:71, P < 0:001) and P. virens (two sample t-test, t ¼ 3:61, P < 0:001) were more abundant during spring as were U. tenuis (ANOVA, F2;65 ¼ 5:80, P < 0:01) and M. tomcod (ANOVA, F2;41 ¼ 7:56, P < 0:001). Others had a more protracted occurrence in our collections with T. adspersus collected during all sampling periods with a September peak, U. chuss and O. mordax abundances peaked in late June–July and August, respectively. Pleuronectes americanus were almost always present but CPUE was highest from late June through October. Pleuronectes americanus were significantly more abundant during summer compared with spring which in turn was greater than autumn (ANOVA, F2;201 ¼ 7:42, P < 0:001). CPUEs of T. adspersus, U. chuss and O. mordax were about equal during the three seasons.
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The overall number of fish species and CPUE differed by depth. More fish species tow1 (ANOVA, F2;413 ¼ 46:4, P < 0:001) were collected at the shallowest depths (between 0.6 and 3 m) followed by intermediate depths (to 6 m) when compared with deeper areas. Overall CPUE for all fishes was highest in shallower water as well (ANOVA, F2;413 ¼ 21:3, P < 0:001). However, CPUE’s of each target species were not significantly different by depth with the exception of T. adspersus which were more abundant in water less than 3 m (ANOVA, F2;59 ¼ 3:98, P < 0:05).
4. Discussion Vegetation was an important component of habitat quality in shallow Maine estuaries. The presence of vegetation, particularly Zostera marina and Laminaria longicruris, had a positive effect on fish species richness and abundance in mid-coast coast estuaries. Casco Bay and the Weskeag River where more vegetated habitats occurred had significantly more fish species tow1 and higher abundances than Muscongus Bay where more unvegetated sandy substrates were present. In all three estuaries, total fish species tow1 and abundances were generally higher in Zostera than nearby unvegetated sandy areas. These findings were consistent with results of other investigations where a more diverse fish community and greater abundance occurred in vegetated areas (Heck et al., 1989; Lazzari & Tupper, 2002; Nixon & Oviatt, 1973; Paterson & Whitfield, 2000; Pearcy & Richards, 1962; Sogard & Able, 1991; Sogard et al., 1987; Szedlmayer & Able, 1996). Laminaria in the Weskeag River and Muscongus Bay also had a positive effect on species richness and abundance but published information does not exist for comparison in this habitat. A number of dominant taxa exhibited clear habitat preferences although there were a few generalist species (i.e. P. gunnellus, P. americanus) that occurred over a variety of substrates. The three Gasterosteid species appeared more restricted in the habitats they utilize to three-dimensional structure such as Zostera and were virtually absent at other habitats. Syngnathus fuscus, T. adspersus, M. aenaeus, and C. lumpus were highly dependent on Zostera but were also present at the unvegetated sites. Only Fundulus heteroclitus and a few other rare species were collected solely in unvegetated habitats. All of the target species except P. americanus and O. mordax occurred more often in areas of vegetation or Microciona than in sandy areas. The attractiveness of Zostera over other habitats has been ascribed to characteristics of seagrass habitat (Bell & Pollard, 1989; Orth et al., 1984). Seagrass canopies provide shade, reduced water currents and increased surface area (Bell & Pollard, 1989) while the rhizome
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mat provided further habitat complexity (Orth et al., 1984). These attributes along with higher primary productivity provided an abundant and varied food supply as well as protection from predators. For example, the predation efficiency of cottids feeding on YOY G. morhua was inversely related to habitat complexity (Tupper & Boutilier, 1995a) and YOY G. morhua kept in aquaria selected more complex substrates in the presence of predators (Gotceitas & Brown, 1993). Thus the relationship between habitat complexity and population density can be attributed to differential predation among habitat types and need not be related to competition for living space. Growth rates of YOY G. morhua in St Margaret’s Bay were higher in seagrass beds than on rocky reef, cobble or sand bottoms (Tupper & Boutilier, 1995b) and were attributed to greater prey densities in seagrass habitat. Larger individuals were rare in our mid-coast coast samples and mainly restricted to presumed age 1+ juvenile P. americanus remaining from the previous year’s recruitment, or adults of species that breed in the immediate environment, such as G. aculeatus and M. aenaeus. Many recreationally and commercially important species such as Anguilla rostrata, Clupea harengus, Gadus morhua, Microgadus tomcod, Pollachius virens, Urophycis chuss, U. regia, U. tenuis, Osmerus mordax, Macrozoarces americanus, T. adspersus, and Pleuronectes americanus used shallow habitats in mid-coast coast Maine estuaries as indicated by the prevalence of their YOY and juveniles in our collections. A similar nursery function has often been observed in marsh systems and other shallow areas elsewhere in the north Atlantic Ocean (Ayvazian et al., 1992; Gibson, Ansell, & Robb, 1993; Heck et al., 1989; Kneib, 1997; Lazzari et al., 1999; Nixon & Oviatt, 1973; Pearcy & Richards, 1962; Sogard & Able, 1991; Weinstein, 1979). For over three decades, about 65% of the coastal fishery resources in the U.S. were thought to be estuarine dependent (McHugh, 1966). However, a revised estimate based on commercial fishery landings indicated that well over 75% by weight of commercially important fishes were dependent of estuaries for reproduction, nurseries, food production or migration (Chambers, 1992) with a much lower percentage (32%) considered estuarine dependent in the northwestern Atlantic Ocean. Heck et al. (1989) found a similar estimate of 34% (by number) of the fish species collected in Nauset Marsh, Cape Cod were either commercially or recreationally important. However, we collected a greater percentage (38%) of these fishes overall and the percentage approached 50% in both Casco Bay (44%) and the Weskeag River (46%). The importance of shallow habitats as nurseries has been demonstrated for species of recreational and commercial importance including G. morhua and P. virens in Canada (Keats, 1986; Keats, South, & Steele, 1987; MacDonald et al., 1984) and in
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Europe (Daan, 1978; Edwards & Steele, 1968; Gibson et al., 1993), but this was the first Maine study to do so. We found YOY G. morhua in all habitats of the three mid-coast estuaries sampled from April through June documenting the importance of these estuarine areas as nurseries on, at least, a seasonal basis. Three other gadoid species (M. tomcod, P. virens, and U. tenuis) of commercial or recreational importance also were common during the spring and YOY U. chuss, T. adspersus, and P. americanus were common components of the fish communities. The shallow habitats sampled in this study were undoubtedly important habitat for gadoids seasonally and for P. americanus almost year-round thus making these fishes susceptible to impacts from coastal pollution and habitat degradation putting the adult fisheries at risk by adversely affecting recruitment. A similar shallow water fish community was observed throughout the northwest Atlantic Ocean from the Canadian Maritimes to Virginia. We compared our results with other habitat studies using seining and trawling methods in Virginia (Orth & Heck, 1980), New Jersey (Szedlmayer & Able, 1996), New York (Briggs & O’Connor, 1971), Connecticut (Warfel & Merrimen, 1944), Rhode Island (Pearcy & Richards, 1962), Massachusetts (Heck et al., 1989), Maine (Ayvazian et al., 1992; Lazzari et al., 1999) and Atlantic Canada (Black & Miller, 1991; MacDonald et al., 1984; Tyler, 1971). As expected, the Maine fish fauna was similar to Massachusetts and intermediate in composition compared with Canada and more southern areas. The fish community in Maine shallow waters consisted primarily of cold temperate species and few of the southern species that add to the faunal richness of New Jersey and Virginia estuaries occurred here. The dominant Maine species of P. americanus, G. aculeatus, A. quadracus, and M. aenaeus had a wide geographic distribution despite important differences in the dominant marsh vegetation, tidal flood regimes, temperature range, and other factors. Seasonal differences in species richness and abundance occurred with peak numbers of species and CPUE occurring in warmer months between June and October in mid-coast coast Maine estuaries. Typically, in northern shallow marine habitats, the summer–autumn assemblage, consisting predominantly of juvenile and small adult fishes, moved from shallow water to offshore habitats in response to declining winter water temperatures (Lazzari et al., 1999; MacDonald et al., 1984; Tyler, 1971) leaving the remaining winter assemblage low in diversity and number and represented by only the most physiologically tolerant species. Seasonal movement from inshore habitat to offshore was important for individual species and resulted in seasonal changes in fish species composition and abundance such that summer–autumn was characterized by a community richer in individuals and species. Seasonal movement from inshore habitat to offshore was unidirectional for
the individual of many species, such as C. harengus and the gadoids, since the shallow water community consisted of a new 0+ yearclass each year. For other species (P. americanus, M. aenaeus), the return inshore was an annual occurrence, triggered by resource availability and predator avoidance (MacDonald et al., 1984). Seasonal movements have been commonly reported elsewhere (Creutzberg & Fonds, 1971; Horn, 1980; Ross, McMichael, & Ruple, 1987) with seasonal patterns within estuaries being attributed to shifts in faunal composition, immigration and emigration from estuaries, and predator–prey interactions (Haedrich, 1983; Nixon & Oviatt, 1973; Rountree & Able, 1992). Other factors contributing to the changes in species number and abundance over time were likely to be emigration into deeper water, as was known to take place in P. americanus (Pearcy, 1962) or a result of the increasing size of many species that made them less vulnerable to our sampling gear. Seasonal patterns in species richness and faunal abundance were observed in Canada (MacDonald et al., 1984; Tyler, 1971), Maine (Ayvazian et al., 1992; Lazzari et al., 1999; Recksiek & McCleave, 1973), Rhode Island (Nixon & Oviatt, 1973), and New Jersey (Rountree & Able, 1992), although the timing of peak species richness and abundance exhibited spatial and annual variation in a particular studies. In summary, fish species richness and faunal abundances were positively associated with vegetation, particularly Zostera ,in three mid-coast coast Maine estuaries. The fish community found in these estuaries was dominated by young-of-the-year and juveniles and all five of the habitats sampled function as nursery areas. A greater percentage of commercial and recreational species was collected in this study than in previous studies in estuaries from the northwest Atlantic Ocean. This study documents the importance of shallow estuarine areas in Maine as nurseries for many commercial and recreational species. Additional research will be needed to determine the relative importance of shallow habitats to the overall recruitment of these fishes. Acknowledgements We would like to thank M. Lucas and J. Lewis for field assistance. This project was funded by the WallopBreaux Trust Fund for Sportfish Restoration. References Adams, S. M. (1976). The ecology of eelgrass, Zostera marina (L.), fish communities. 1. Structural analysis. Journal of Experimental Marine Biology and Ecology 22, 269–291. Ayvazian, S. G., Deegan, L. A., & Finn, J. T. (1992). Comparison of habitat use by estuarine fish assemblages in the Acadian and Virginian zoogeographic provinces. Estuaries 15, 368–383.
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