Rachel B. McDonald, Ryan M. Moody, Ken L. Heck & Just Cebrian

Transcription

1 Fish, Macroinvertebrate and Epifaunal Communities in Shallow Coastal Lagoons with Varying Seagrass Cover of the Northern Gulf of Mexico Rachel B. McDonald, Ryan M. Moody, Ken L. Heck & Just Cebrian Estuaries and Coasts Journal of the Coastal and Estuarine Research Federation ISSN Volume 39 Number 3 Estuaries and Coasts (2016) 39: DOI /s

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3 Estuaries and Coasts (2016) 39: DOI /s Fish, Macroinvertebrate and Epifaunal Communities in Shallow Coastal Lagoons with Varying Seagrass Cover of the Northern Gulf of Mexico Rachel B. McDonald 1,2 & Ryan M. Moody 1,2 & Ken L. Heck 1,2 & Just Cebrian 1,2 Received: 2 May 2014 /Revised: 14 August 2015 /Accepted: 31 August 2015 /Published online: 5 November 2015 # Coastal and Estuarine Research Federation 2015 Abstract Coastal lagoons are ubiquitous along coastlines worldwide. Here, we compare the abundance of epifauna, seagrass-associated macroinvertebrates, and small fish across a gradient of seagrass cover in shallow coastal lagoons of the northern Gulf of Mexico. Two of the lagoons had little or no seagrass cover ( %), and four had high cover ( %). All of the lagoons were partially covered with fringing marsh. We hypothesized that, due to habitat redundancy between seagrass beds and fringing marshes, seagrassassociated fish and macroinvertebrates would not be largely reduced despite the large differences in seagrass cover among the lagoons. Our results support this hypothesis. For most sampling dates, we did not find significant differences in fish and macroinvertebrate abundance among the lagoons and, when we did, several highly vegetated lagoons did not have larger abundances than sparsely vegetated lagoons. The extreme shallowness of the lagoons studied (<1 m) may also provide further protection from large predatory fishes in the absence of seagrasses. Our results also suggest that marsh detritus, by providing habitat for epifauna and helping maintain prey availability, may further temper reductions in seagrass-associated fishes and macroinvertebrates following seagrass decline. The results highlight the importance of Communicated by Karin E. Limburg Electronic supplementary material The online version of this article (doi: /s ) contains supplementary material, which is available to authorized users. * Rachel B. McDonald rmcdonald@disl.org 1 2 Dauphin Island Sea Lab, Dauphin Island, AL, USA Department of Marine Sciences, University of South Alabama, Mobile, AL, USA marsh-bordered, shallow lagoons as habitat for small fish and macroinvertebrates regardless of seagrass cover. This study contributes to the characterization of habitat redundancy in coastal ecosystems and pinpoints the importance of considering all habitats in concert for the proper understanding and management of coastal ecosystems. Keywords Coastal lagoons. Seagrass. Nekton. Epifauna. Fringing marsh. Gulf of Mexico Introduction Lagoons occupy approximately 13 % of coastlines worldwide, with the largest extent along the Atlantic and Gulf coasts of the USA, where they cover approximately 2800 km of shoreline (Kennish and Paerl 2010). Lagoons are often protected by a barrier island, spit, reef, or sand bank and connected to the open ocean by tidal inlets. Coastal lagoons are also characterized by shallow waters that generally average less than 2 m in depth, although channels and relict holes may be deeper. Unlike estuaries, coastal lagoons do not normally feature riverine inputs and freshwater mainly enters the lagoon via surface runoff and groundwater (Lehrter and Cebrian 2010). Seagrass meadows are ubiquitous in shallow coastal waters, including lagoons, and function as critical habitat for many finfish and shellfish species (Beck et al. 2001; Williams and Heck 2001). The faunal assemblages that inhabit seagrass beds have been well documented and include both resident and transient species. Many transient species have complex life cycles and are seasonal recruits, the majority of which are juvenile fish and decapod crustaceans that later migrate offshore or to other habitats where they become adults (Heck et al. 2008). In coastal waters of the northern Gulf of Mexico,

4 Estuaries and Coasts (2016) 39: examples of resident species include rainwater killifish (Lucania parva), blue crab (Callinectes sapidus), and grass shrimp (Palaemonetes pugio) (Jordan2002; Thomasetal.1990; Welsh 1975), and transient species include pinfish (Lagodon rhomboides), red drum (Sciaenops ocellatus) and penaeid shrimp species (Farfantepenaeus aztecus and Litopenaeus setiferus) (Minello and Zimmerman 1983; Nelsonetal. 2013; Phillips et al. 1989; Rooker and Holt 1997). Seagrasses have been declining worldwide due to natural and anthropogenic processes (Waycott et al. 2009). Natural events include waves and storms, while anthropogenic factors include dredging, harbor construction, pollution, disease, and vessel damage (Orth et al. 2006; Short and Wyllie-Echeverria 1996). Although seagrass beds naturally occur as vegetated patches interspersed with bare sediment, anthropogenic damage has further fragmented seagrass beds, increasing the area of bare sediment in coastal waters (Johnson and Heck 2006). A decline in seagrass beds may therefore negatively impact species that inhabit the beds and require this habitat for growth and survival, such as the resident and transient species mentioned previously (Cebrian et al. 2009a; Hughesetal.2009). Fringing marsh is also a ubiquitous component of coastal lagoons, and there may be significant habitat complementarity between seagrass beds and fringing marshes in coastal lagoons. Rozas and Minello (1998) found that seagrass meadows could provide an alternative habitat at low tide for marsh species when the marsh platform was not accessible. Similarly, seagrass-associated nekton can access fringing marsh vegetation for food and refuge at high tide while the marsh platform is flooded (Minello et al. 2012; Moody et al. 2013a; Rozas et al. 2012). Therefore, habitat complementarity between seagrass beds and surrounding fringing marsh could mitigate reductions in fish habitat following declines in seagrass abundance. Many species that frequent coastal lagoons are not common in seagrass beds. For instance, Hughes et al. (2002) found that fish assemblages differed substantially between seagrass and bare bottom sites in New England coastal lagoons, with benthic species such as oyster toadfish (Opsanus tau), mummichog (Fundulus heteroclites), and grubby sculpin (Myoxocephalus anaeus) being the most abundant in seagrass sites, and pelagic schooling species such as bay anchovy (Anchoa mitchilli), Atlantic silverside (Menidia menidia), and scup (Stenotomus chrysops) being dominant in bare sediment sites. Minello et al. (2003) found that pinfish were more associated with vegetated areas whereas gulf menhaden (Brevoortia patronus), spot (Leiostomus xanthurus), and spotfin mojarra (Eucinostomus argenteus) weremoreassociated with non-vegetated areas. Therefore, species that are not seagrass-associated may be minimally affected by seagrass loss in coastal habitats and may become the dominant species of the community following seagrass loss. The response of fish communities to varying seagrass cover in shallow coastal lagoons has not been as well studied as in other coastal systems that typically have greater depths, such as bays and estuaries (Able et al. 2011; Heck et al. 1989; Hughes et al. 2002; Valesini et al. 2004). We hypothesized that seagrass-associated fish and macroinvertebrate species may not always endure large declines with reduced seagrass habitat in shallow lagoons surrounded by fringing marsh as the fringing marsh may provide habitat redundancy and compensate for seagrass loss. In addition, extreme shallowness in the lagoons may limit access by large fish, which would offer additional protection to small fishes (Rozas and Minello 1998). To test this hypothesis, we compared the abundance and species composition of fish, macroinvertebrates, and epifaunal organisms over 2 years in six extremely shallow lagoons located in the northern Gulf of Mexico that were bordered with fringing marsh and had varying degrees of seagrass cover. Methods Study Sites We selected six shallow lagoons with varying seagrass cover (Spanish Cove, Langley Point, State Park, Kee s Bayou,Joe s Site and Gongora) in Big Lagoon (Florida, USA). Within each lagoon, we selected a sampling area that was representative of the entire lagoon (Fig. 1). The only exception was Kee s Bayou, where we selected the vegetated north-western part of the lagoon for sampling as seining was not possible on the soft, silty bottom of the south-eastern part (Cebrian et al. 2009a; Stutes et al. 2007). All samples were taken within the sampling area. On each sampling date, we took eight cores haphazardly within each sampling area along with the seine and suction samples (see below) and calculated the percent of cores that had seagrass. The mean percent of cores with seagrass for the entire study duration ranged from 0 to 97.3 % across lagoons (Table 1). The two easternmost lagoons, Spanish Cove and Langley Point, are dominated by turtlegrass (Thalassia testudinum) with interspersed patches of shoalgrass (Halodule wrightii). State Park and Joe s Site features H. wrightii as the dominant species with interspersed patches of widgeon grass (Ruppia maritima), whereas Kee s Bayou has a higher abundance of R. maritima than H. wrightii. A large fraction of the shoreline in the lagoons is bordered with fringing saltmarsh (Table 1). In all lagoons, the fringing saltmarsh had a band of cordgrass (Spartina alterniflora) at the waterfront edge and a strip of black needlerush (Juncus roemerianus) landward of the cordgrass.

5 720 Estuaries and Coasts (2016) 39: Fig. 1 Map of the lagoons studied; top row, left to right:kee s Bayou and State Park; bottom row, left to right:gongora,joe s Site, Langley Point, and Spanish Cove. Yellow lines delineate the areas sampled within the lagoons Variables Measured The study was carried out from April 2010 to January Sampling was conducted every other month from April to October with additional sampling in January. In shallow coastal lagoons of the northern Gulf of Mexico, most juvenile recruitment occurs in winter/early spring. Juveniles remain in the lagoons through spring and summer, and the majority migrate offshore with the arrival of cold fronts in fall (Cebrian et al. 2009a; Middaugh and Hemmer 1992; Nelson 2002). Therefore, this sampling timeline allowed us to capture the magnitude of winter/spring recruitment and fall migration. Environmental Measurements We measured water-column depth, temperature, salinity, and dissolved oxygen concentration. These measurements were taken at three haphazardly selected locations within the sampling area of each lagoon on each sampling date. Depth was measured with a meter stick, and temperature, salinity, and dissolved oxygen were measured at the mid-water-column with a hand-held YSI 85. Seining Fish and large macroinvertebrates were collected using a 6.0 m 1.5 m bag seine with 3 mm mesh. Three haphazardly located seines were pulled for 20 m within the sampling area of the lagoon on each collection date. A core (15.5 cm diameter) was taken at the center of the seine transect to assess seagrass cover in the sampling area (Table 1). The seine samples were taken to the laboratory for processing. All fish and macroinvertebrates were identified and counted. Fish were measured for standard and total length, and macroinvertebrates were measured from rostrum to telson (e.g., penaeid shrimp) or across the carapace (e.g., crabs). Due to overlapping spawning seasons and the timing of molting, it is likely that we misidentified a few white shrimp (L. setiferus) as brown shrimp (F. aztecus) and the two species were therefore grouped as penaeid shrimp.

6 Estuaries and Coasts (2016) 39: Table 1 Environmental data, seagrass cover and fraction of lagoon perimeter bordered with fringing marsh. Percent cover is calculated as the percent of the eight cores taken on each sampling date that had seagrass (see BStudy Sites^). Environmental data encompass all sampling dates except April 2010 for dissolved oxygen, salinity, and temperature Dissolved oxygen Salinity Temperature Fraction of perimeter bordered by marsh Marsh border (m) Perimeter of the sampled area (m) Dept (m) mg/l % ppt C Percent cores with seagrass Site Range Mean (±SE) Range Mean (±SE) Range Mean (±SE) Range Mean (±SE) Range Mean (±SE) Range Mean (±SE) Spanish Cove (±0.0) (±0.6) (±9.1) (±1.1) (±2.4) (±2.5) Kee s Bayou (±0.05) (±0.6) (±8.0) (±1.3) (±2.2) (±2.8) State Park (±0.05) (±0.3) (±7.2) (±1.0) (±2.4) (±5.8) Langley Point (±0.06) (±0.6) (±8.2) (±0.9) (±2.1) (±4.9) Joe s Site (±0.06) (±0.7) (±9.2) (±1.1) (±2.2) (±5.7) Gongora (±0.05) (±0.6) (±7.7) (±0.8) (±2.2) Suction Sampling Epifaunal invertebrates were collected using a suction sampler following specifications for shallow systems (Heck et al. 2001). Five samples were collected haphazardly within the sampling area of the lagoon on each sampling date. Briefly, samples were taken by placing an open ended cylinder (1.6 m high, 52.1 cm wide) onto the sediment and creating a tight seal by pressing the cylinder into the sediment. Care was taken not to disturb the sampling area prior to cylinder placement. Subsequently, the epifauna enclosed within the cylinder was suctioned out and collected with a 0.5 mm mesh bag. The area enclosed by the cylinder was swept with a hand net after suctioning to ensure that most epifauna were collected. In addition, we collected a core (15.5 cm diameter) haphazardly around the cylinder margin to determine seagrass cover in the sampling area (Table 1). The samples were transported to the laboratory on ice and frozen for later examination. Upon thawing, the samples were dyed with Rose Bengal and separated into major taxonomic groups for identification and abundance counts. The groups were amphipod, isopod, gastropod, mysid, paguridae, tanaid, echinoderm, Bshrimp^ (penaeid, alpheidae, and other carideans), and Bcrab^ (xanthidae and portunidae). Clipping Experiment Our hypothesis was that, in shallow coastal lagoons surrounded with fringing marsh, the abundance of seagrassassociated fish and macroinvertebrate species would not drastically be reduced with decreased seagrass cover due to habitat complementarity offered by the fringing marsh. Seagrass decline should cause the loss of refuge and food (i.e., epiphytes and epifauna) for seagrass-associated species but, if fringing marshes offset that loss due to habitat complementarity, then we should not find large decreases in the abundance of seagrass-associated species. To test this hypothesis, we have measured both the abundance of seagrass-associated fish, large macroinvertebrates, and epifauna in lagoons with varying seagrass cover. We expect large reductions in epifaunal abundance with decreased seagrass cover, but not necessarily in fish and large macroinvertebrate abundance. In addition, to further test how epifauna abundance changes with reduced seagrass cover, we carried out a clipping experiment in the lagoon with the highest seagrass cover (Spanish Cove) starting in April of the second year. At each sampling time (i.e., bimonthly April-October), all seagrass in five fixed 1 m 2 plots located within the lagoon sampling area were clipped with scissors at the base of the leaves. One day after clipping, suction sampling was carried out in the clipped plots and in vegetated areas haphazardly located in the lagoon as described above. To account for edge effects, the size of the trimmed

7 722 Estuaries and Coasts (2016) 39: plots was 50 cm larger than the diameter of the suction sampling cylinder. Samples from the trimmed plots were processed in the same fashion as samples from the adjacent vegetated areas (see 2.2c BSuction Sampling^). We also compared epifaunal abundance in the clipped plots (which still had the base of the shoots present) with the abundance measured in Gongora, the lagoon with no seagrass, to gain further insight of how reduced structure affects epifaunal abundance. Statistical Analyses Abundance data for fish, large macroinvertebrates, and epifauna were analyzed using a mixed two-way analysis of variance (ANOVA) with Blagoon^ as a fixed factor and Bsampling time^ as a random factor. If lagoon was significant in the two-way ANOVA and both sampling time and the interaction between lagoon and sampling time were not, sampling times were pooled for each lagoon and the lagoons compared with one-way ANOVA followed by Tukey tests. If the interaction was significant regardless of whether lagoon or sampling time were significant or not, or if lagoon and sampling time were significant and the interaction was not, oneway ANOVA and Tukey comparisons among lagoons were done separately for each sampling time (Quinn and Keough 2002). Abundances were square root transformed to comply with the assumptions of ANOVA. Despite the square root transformation, ANOVA assumptions were not fully met in some cases and the α value was lowered to to reduce the chances of committing type I error. To examine whether differences in fish and macroinvertebrate individual size existed across lagoons, we compared our individual length measurements among lagoons for each sampling date with a one-way ANOVA followed by Tukey tests. Comparisons among lagoons were done for each sampling date separately as most species had sampling dates where we captured no individuals in some lagoons. Length data were square root transformed and the α value lowered to ANOVA was conducted using the Minitab 14 statistical software. Seining is regarded as an adequate technique to capture macroinvertebrates and small individuals of fish species associated with seagrass structure (Rozas and Minello 1997, 1998). However, seining may not adequately sample pelagic schooling species, such as gulf menhaden and bay anchovy (Rozas and Minello 1997); therefore, we did not consider those species in our analysis. Furthermore, we only collected three 6.0 m 1.5 m bag seines at each lagoon on each sampling time, with each seine covering a 20 m transect; this sampling effort may have been too low for non-abundant species (Cebrian et al. 2009a). Therefore, we focused our analyses on ten abundant seagrass-associated species of fish and macroinvertebrates that are considered to be adequately sampled with seining. These species allow for a strong test of how seagrass-associated species respond to decreasing seagrass cover in shallow coastal lagoons surrounded with fringing marsh and whether there is evidence of habitat complementarity between seagrass beds and adjacent fringing marshes. Results Environmental Measurements Mean depth was <1 m in the areas sampled within the lagoons. The areas ranged widely in seagrass cover (Table 1), with four lagoons (Spanish Cove, Kee s Bayou, State Park, and Langley Point) having high seagrass cover ( %), one (Joe s site) having low cover (18.8 %), and one (Gongora) having no seagrass. Water temperature reflected typical seasonal variability, with values ranging from ca. 13 to 35 C. Salinity values varied between mesohaline and euhaline conditions, as typically found in Big Lagoon (Stutes et al. 2007). Our measurements of oxygen concentration during daytime reflected well-oxygenated waters. Mean values of oxygen concentration, salinity, and temperature were similar among the lagoons. Fish and Macroinvertebrate Abundance A diverse assemblage of fish and macroinvertebrates totaling 108,234 individuals was collected during this study. We captured 55 species of fish and 8 taxa (identified to genus or species level) of macroinvertebrates (Electronic Supplementary Material 11). We focused our analyses on ten seagrass-associated species or taxa that are adequately captured with seining (see 2.3 BStatistical Analyses^). These species are grass shrimp, pinfish, rainwater killifish (Lucania parva), penaeid shrimp, blue crab, inland silverside (Menidia beryllina), clown goby (Microgobius gulosus), spotfin mojarra, code goby (Gobiosoma robustum), and darter goby (Ctenogobius boleosoma) (Table 2). We also included spot (Leiostomus xanthurus), a non seagrass-associated species captured in high abundance. We did not find a strong tendency for seagrass-associated species to have higher abundances in the highly seagrassvegetated lagoons than in the sparsely vegetated lagoons (Table 3; Fig. 2a, b; Electronic Supplementary Material 2 10). We found a significant interaction between lagoon and sampling time for grass shrimp, pinfish, rainwater killifish, penaeid shrimp, inland silverside, clown goby and code goby. For blue crabs, both main time and lagoon effects were significant, but the interaction was not. When lagoons were compared separately for each sampling date for each of these species, we found a common outcome; significant differences were not found among the lagoons on most dates, and when we did, several of the highly vegetated lagoons did not have significantly higher

8 Estuaries and Coasts (2016) 39: Table 2 Species analyzed. Total counts for all lagoons and all sampling dates are provided. Information on their life history (spawning, recruitment, and movement) is also provided Species n Spawning Recruitment Movement Literature Grass shrimp (Palaemonetes pugio) 49,236 Late spring through fall Resident Annual species (13 month life span) Anderson 1985; Welsh1975 Pinfish (Lagodon rhomboides) 18,125 Late fall to early spring offshore (some may occur inshore) Juveniles enter estuaries late winter through spring Migrate out of estuaries late fall Muncy 1984; Nelson2002 Rainwater killifish (Lucania parva) 8141 Early summer Resident Migrate to fresh water to breed Moyle 1976; Jordan2002 Penaeid shrimp (Farfantepenaeus aztecus and Litopenaeus setiferus) 4152 Offshore F. aztecus: September May, but can occur year round L. setiferus: April-October Blue crab (Callinectes sapidus) 2959 Estuarine and coastal occurs spring through summer Estuarine recruitment begins 2 3 weeks after spawning Estuarine recruitment occurs from summer to early winter Inland silverside (Menidia beryllina) 1607 Spring in upper estuary YOY found in upper estuary during summer Both species migrate at maturity from winter-spring F. aztecus migrates offshore L. setiferus migrates to nearshore waters Females migrate down estuary in fall; juveniles and males move into deeper water over winter Migrate to lower estuary in fall at mm Clown goby (Microgobius gulosus) 1064 Springtolatefall Resident No migration; adults burrow over winter Spotfin mojarra (Eucinostomus argenteus) 982 Suggested to be during the warmer months Code goby (Gobiosoma robustum) 695 Late spring to early summer and late summer to early fall Juveniles found in lagoons and inshore areas seasonally Found in or around inlets in warmer months Resident No migration; annual fish (1-year life span) Lassuy 1983; Lindner and Anderson 1956; Minello and Zimmerman 1983 Hines and Ruiz 1995; Hines 2007; Perry and McIlwain 1986; Thomasetal.1990; Murphy et al Gleason and Bengtson 1996 Gaisner 2005 Kerschner et al. 1985; Livingston 1984; Richards2004 Springer and McErlean 1961 Darter goby (Ctenogobius boleosoma) 661 Suggested to peak in mid summer Resident No migration Hendon et al. 2001; Hildebrand and Cable 1938 Spot (Leiostomus xanthurus) 12,339 Offshore from fall to early spring Winter through early spring Fall offshore migration for spawning Boesch and Turner 1984; Phillips et al. 1989

9 724 Estuaries and Coasts (2016) 39: Table 3 ANOVA results for fish and macroinvertebrate abundance. Results from Tukey analyses are depicted in Fig. 2 as pertinent (see text) Date p value Lagoon p value D L p value Grass shrimp Pinfish Rainwater killifish Penaeid shrimp Blue crab Inland silverside Clown goby Spotfin mojarra Code goby Darter goby Spot abundances than the sparsely vegetated lagoons. For spotfin mojarra, we did not find any significant differences among lagoons on any sampling date. Dates were pooled for the comparison across lagoons for darter goby since both the main time effect and the interaction were not significant. For this species, we also found that several highly vegetated lagoons did not significantly have higher abundance than the sparsely vegetated lagoons. The abundance of spot, a species with little association to seagrasses, varied over time but not across lagoons (Table 3; Electronic Supplementary Material 10). Fish and Macroinvertebrate Size We did not find clear and consistent differences in individual size between high and low seagrass-vegetated lagoons for the fish and macroinvertebrate species examined. Pinfish tended to be larger in Gongora (no seagrass cover) than most other lagoons during summer and fall (Table 4; Fig. 3a). The size of rainwater killifish was often larger in Spanish Cove (a highly vegetated lagoon) in relation to other lagoons (Table 4; Fig.3b). For most species, size histograms reflected the temporal dynamics of recruitment and growth through the year. Pinfish were smallest in January and generally increased in size during the subsequent months to reach maximum values in fall (Fig. 3a). Large rainwater killifish occurred year round, whereas small individuals were mainly found in June, August and January (Fig. 3b). For penaeid shrimp, however, no consistent differences in size were found through time (Electronic Supplementary Material 11). Blue crabs were smallest in January, although many small blue crabs were also found in other months, and large adults were mainly found in summer (Electronic Supplementary Material 12). No clear temporal pattern was evident for the size of inland silversides, although Fig. 2 Abundance (individuals per square meter) of abundant species of seagrass-associated macroinvertebrates and small fish. a grass shrimp; b pinfish. Before plotting, 1 was added to each abundance value and this sum was log transformed. Plotted values denote the mean for each lagoon and sampling date, and the line on the values denotes ± SE. Tukey comparisons among lagoons are shown as pertinent (i.e., for each sampling date separately or pooling all dates together, see text). Green symbols correspond to highly vegetated lagoons, and orange symbols to sparsely vegetated lagoons (see text): S Spanish Cove, K Kee s Bayou, P State Park, L Langley Point, J Joe s Site,G Gongora, ns non-significant numerous small fish were found in some lagoons in January (Electronic Supplementary Material 13). Small clown gobies were mainly found in June and October (Electronic Supplementary Material 14). Spotfin mojarra displayed both the smallest and largest individuals in August and October, with intermediate sizes in the other months (Electronic Supplementary Material 15). Code gobies were generally smallest in October and January and largest in April and June (Electronic Supplementary Material 16). We generally found larger darter gobies in June and smaller ones in January during the first year of the study (Electronic Supplementary Material 17). Spot were smallest in January and grew over time to reach maximum values in fall (Electronic Supplementary Material 18).

10 Estuaries and Coasts (2016) 39: Table 4 ANOVA results for individual fish length. Lagoons are compared for each sampling date. Corresponding Tukey comparisons are depicted in Fig. 3 and ESM 2 9. In a few cases (i.e., blue crab in January 2011 and October 2011; clown goby in April 2010; and darter goby in April 2010 and October 2010), we did not find significant pairwise differences with the Tukey comparisons despite obtaining a significant one-way ANOVA. na not applicable (we did not capture two or more individuals in at least two of the lagoons on the given date) April 2010 June 2010 August 2010 October 2010 January 2011 April 2011 June 2011 August 2011 October 2011 January 2012 Pinfish Rainwater killifish Penaeid shrimp Blue crab Inland silverside Clown goby n.a Spotfin mojarra n.a. n.a n.a. n.a n.a. Code goby n.a. n.a Darter goby n.a. n.a Spot Epifaunal Abundance All nine epifaunal groups displayed a significant interaction between lagoon and sampling time (Fig. 4a, b; Electronic Supplementary Material 19 25; Table 5). When abundance was compared among lagoons separately for each sampling date, we found significant differences on one out of ten sampling dates for crabs and mysids (Electronic Supplementary Material 21, 24); three dates for echinoderms (Electronic Supplementary Material 25); four dates for amphipods and isopods (Fig. 4a, b); five dates for paguridae and tanaids (Electronic Supplementary Material 22, 23); six dates for shrimp (Electronic Supplementary Material 19); and eight dates for gastropods (Electronic Supplementary Material 20). The sum of the abundance of all nine groups displayed significant differences among the lagoons on seven sampling dates (Electronic Supplementary Material 26). For all sampling dates where significant differences were found among lagoons, several highly seagrass-vegetated lagoons did not have higher abundances than the sparsely vegetated lagoons (Fig. 4a, b; Electronic Supplementary Material 19 26). Clipping Experiment We found reduced epifaunal abundance in clipped compared to non-clipped plots in Spanish Cove on three out of the four sampling dates (Fig. 5). We found reduced epifaunal abundance in Gongora in relation to clipped plots in Spanish Cove in two out of the four sampling dates (Fig. 5). Discussion This study examines the abundance of ten seagrass-associated species of macroinvertebrates and small fish in six extremely shallow coastal lagoons (mean depth < 1 m) in the northern Gulf of Mexico. The areas sampled in the lagoons featured contrasting levels of seagrass cover, with four having high cover ( %) and two having no or low cover ( %), but all of them surrounded in part with fringing marsh. Our hypothesis was that the abundance of these species would not consistently and largely be reduced in low vegetated in relation to high vegetated lagoons owing to habitat redundancy provided by the surrounding marsh and additional protection against large fish offered by their extreme shallowness (Minello et al. 2012; Moody et al. 2013a; Rozas and Minello 1998; Rozas et al. 2012). Our results support this hypothesis. For all those species, we found no significant differences in abundance among the lagoons on most sampling dates and, when we did, several highly vegetated lagoons did have larger abundances than sparsely vegetated lagoons. Thus, the ten seagrass-associated species studied here were often as abundant in low vegetated lagoons as they were in high vegetated lagoons. The abundance of spot, a non seagrass-associated species, did not vary across lagoons. Thetypeofdominantseagrassdidnotseemtoaffectour conclusion. Spanish Cove and Langley Point had mostly turtlegrass and some patches of shoalgrass. Shoalgrass was dominant in State Park and Joe s site, where some widgeon grass also occurred. Widgeon grass was dominant in Kee s Bayou, where some shoalgrass also occured. Thus, sparsely vegetated lagoons often had similar abundances of seagrassassociated fish and macroinvertebrates as did highly vegetated Fig. 3 Individual length histograms. a pinfish; b rainwater killifish. Values on the y-axis denote the percent of individuals captured, and values on the x-axis correspond to length expressed in mm. Tukey comparisons among lagoons are shown above corresponding sampling dates (see Table 4). Symbols as in Fig. 2. ns non-significant, na not applicable (we did not capture two or more individuals in at least two of the lagoons on the given date)

11 726 Estuaries and Coasts (2016) 39:

12 Estuaries and Coasts (2016) 39: Table 5 ANOVA results for epifauna abundance. Results from Tukey analyses are depicted in Fig. 4 as pertinent (see text) Date p value Lagoon p value D L p value Amphipod Isopod Shrimp Gastropod Crabs Paguridae Tanaid Mysid Echinoderm Total Fig. 4 Abundance of epifauna captured with suction sampling. a amphipods; b isopods. Before plotting, 1 was added to each abundance value and this sum was log transformed. Plotted values denote the mean for each lagoon and sampling date, and the line on the values denotes ± SE. Tukey comparisons among lagoons are shown for each sampling date separately (see text). Symbols as in Fig. 2. ns non-significant (Boesch and Turner 1984; Irlandi and Crawford 1997; Minello et al. 2012). In particular, the transitional slope between the seaward limit of the marsh and open water of the lagoon is a Bhotspot^ used by many fish and macroinvertebrates for refuge and food, including the species considered in this study (Moody et al. 2013a; Rozas and Minello 1998; Stunz et al. 2010). The marsh may also transition into lagoonal open water as a steep escarpment, which features high levels of structural complexity that can provide shelter for numerous organisms (Boesch and Turner 1984; Minello et al. 2003; Moody et al. 2013b). In addition, the marsh platform can also become habitat for many fish and macroinvertebrates when lagoons regardless of the dominant seagrass species in the highly vegetated lagoon. Previous research has found that differences in structural complexity among seagrass species may lead to differences in the abundance and type of associated fauna (Boström et al. 2006; Connolly and Hindell 2006), but here, we do not find large and consistent differences in seagrass-associated fauna density among highly vegetated lagoons dominated by different seagrass species or between those lagoons and low vegetated (including one lagoon with no seagrass) lagoons. Our findings should not be affected by lagoon accessibility to new fish and macroinvertebrate recruits since all lagoons have well connected mouths to the same large body of water, Big Lagoon, which in turn is connected with a wide passage to the open waters of the Gulf of Mexico. The lagoons studied here are partly bordered by fringing marsh, and it is well known that fringing marsh constitutes habitat for many species of fish and macroinvertebrates Fig. 5 Total epifaunal abundance (sum of the nine groups shown in Fig. 4) in non-clipped and clipped plots in Spanish Cove and in Gongora. Bars correspond to mean values and lines to ± SE. Abundance was compared between non-clipped and clipped plots, and between clipped plots and Gongora for each time separately with a t test. Data were square root transformed and met the conditions of normality and homocedasticity. Asterisks denote significant differences at p 0.05

13 728 Estuaries and Coasts (2016) 39: flooded at high tides. For instance, blue crabs, penaeid shrimp, grass shrimp, pinfish, darter goby, rainwater killifish, and inland silverside may dwell on the marsh platform when it is submerged at high tide (Peterson and Turner 1994; Rozas and Minello 1998). Indeed, prior work has indicated that fringing marshes can act as redundant habitats to seagrass beds (Minello et al. 2012; Rozas and Minello 1998; Rozas et al. 2012). The extreme shallowness of the lagoons studied may constitute another mechanism by which these lagoons provide refuge regardless of the amount of seagrass cover. We never measured water depths greater than 1 m in any of the lagoons, although depths greater than 1 m are possible on extremely high tides (Cebrian et al. 2009a). Measured depths ranged from 24 to 98 cm, and mean depths were 80 cm. Such shallow conditions could significantly restrict access by large predatory fish, thereby providing protection to macroinvertebrates and small fish. Accordingly, it has been shown that predation risk for small fish increases with depth (Hines and Ruiz 1995; Rozas and Minello 1998; Ruizetal.1993). Unlike the ten seagrass-associated species of fish and macroinvertebrates studied, we expected a decrease in epifaunal abundance with reduced seagrass abundance. The clipping experiment in Spanish Cove, a highly vegetated lagoon, did show lower epifaunal abundance in clipped compared to nonclipped plots on three out of the four dates the experiment was carried out. However, the results from the epifaunal abundance survey in the lagoons were somewhat equivocal. Out of our ten sampling dates, we found differences in abundance among lagoons on one date for crabs and mysids, three dates for echinoderms, four dates for amphipods and isopods, five dates for paguridae and tanaids, six dates for shrimp, and eight dates for gastropods. Furthermore, several highly vegetated lagoons did not have larger abundances than sparsely vegetated lagoons on the dates where we found differences among lagoons. Overall, these results indicate many instances during our 2-year survey where the abundance of these epifaunal groups was not higher in highly vegetated than in sparsely vegetated lagoons, despite the large differences in seagrass cover that existed between these two groups of lagoons. While the reasons remain unclear, we suggest the lack of large and consistent differences in epifaunal abundance with reduced seagrass cover among the lagoons compared to be partially explained by marsh detritus that falls onto the bottom of the lagoons. Marsh detritus is a common feature on the bottom of the lagoons studied (Cebrian et al. 2009b; Ferrero- Vicente et al. 2011;Stutesetal.2007), and the debris may be habitat for epifaunal organisms particularly in lagoons with little or no seagrass. The comparison between Gongora, a lagoon without seagrass, and clipped plots in Spanish Cove, offers support to this suggestion. Clipped plots were left with the base of the seagrass shoots, which still provided some structure for epifauna. Out of the four dates compared, epifaunal abundance was higher in the clipped plots in Spanish Cove than in Gongora on two dates but not on the other two dates. By providing habitat for epifauna, the occurrence of marsh detrital debris in Gongora may help explain why epifauna abundance did not differ between this lagoon and the clipped plots in Spanish Cove on half of the dates compared. In addition, marsh detrital debris, through helping maintain prey availability, may help temper declines in seagrassassociated fish and macroinvertebrates following seagrass decline. We did not find any consistent differences in individual size of the seagrass-associated fish and macroinvertebrates studied between highly and sparsely seagrass-vegetated lagoons. In general, temporal changes in the size distribution of the species studied reflected its life history and patterns of recruitment and movement in coastal systems. In what follows, we discuss a few examples. The mean size of pinfish was smallest in January and increased through spring, summer, and fall, consistent with their recruitment to coastal systems in winter, residence through spring and summer, and migration offshore in fall (Cebrian et al. 2009a; Nelson et al. 2013). We observed large abundances of small blue crabs in January, consistent with the majority of recruitment occurring in summer to late fall (Hines 2007;Murphy et al.2007;thomas et al. 1990), and large individuals in summer, consistent with spawning seasons from spring to fall and the migration of larger juveniles and adults to deeper waters in fall/early winter (Hines and Ruiz 1995; Perry and McIlwain 1986). Code gobies were largest in spring and summer, and smallest in fall and winter, consistent with a spawning period from late spring to early fall and their annual life cycle (Springer and McErlean 1961). Similar to pinfish, spot was smallest in January and increased in mean size through spring and summer to reach maximum size in fall, which is consistent with their recruitment to coastal waters in winter, residence throughout the spring and summer, and migration offshore in fall as temperature drops (Phillips et al. 1989). In conclusion, our study provides evidence of habitat redundancy between seagrass beds and fringing marshes for seagrass-associated species of fish and macroinvertebrates in shallow coastal lagoons. Such redundancy may partially offset declines of these species following seagrass loss. Extreme shallowness may also contribute to providing refuge from large predators in the absence of seagrasses. Marsh detrital debris, through providing habitat for epifauna and helping maintain prey availability, may also temper declines in seagrass-associated fish and macroinvertebrates following seagrass decline. These results highlight the important role of marsh-bordered, shallow lagoons as habitat for small fish and macroinvertebrates regardless of seagrass cover. Further studies on extent, regulation, and implications of habitat redundancy in coastal ecosystems will improve our

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