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Estuaries and CoastsJournal of the Coastal and EstuarineResearch Federation ISSN 1559-2723Volume 39Number 3 Estuaries and Coasts (2016) 39:718-730DOI 10.1007/s12237-015-0031-7
Fish, Macroinvertebrate and EpifaunalCommunities in Shallow Coastal Lagoonswith Varying Seagrass Cover of theNorthern Gulf of Mexico
Rachel B. McDonald, Ryan M. Moody,Ken L. Heck & Just Cebrian
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Fish, Macroinvertebrate and Epifaunal Communities in ShallowCoastal Lagoons with Varying Seagrass Cover of the NorthernGulf of Mexico
Rachel B. McDonald1,2& Ryan M. Moody1,2 & Ken L. Heck1,2
& Just Cebrian1,2
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 coastlinesworldwide. Here, we compare the abundance of epifauna,seagrass-associated macroinvertebrates, and small fish acrossa gradient of seagrass cover in shallow coastal lagoons of thenorthern Gulf of Mexico. Two of the lagoons had little or noseagrass cover (0–18.8 %), and four had high cover (83.8–97.5 %). All of the lagoons were partially covered with fring-ing marsh. We hypothesized that, due to habitat redundancybetween seagrass beds and fringing marshes, seagrass-associated fish and macroinvertebrates would not be largelyreduced despite the large differences in seagrass cover amongthe lagoons. Our results support this hypothesis. For mostsampling dates, we did not find significant differences in fishand macroinvertebrate abundance among the lagoons and,when we did, several highly vegetated lagoons did not havelarger abundances than sparsely vegetated lagoons. The ex-treme shallowness of the lagoons studied (<1 m) may alsoprovide further protection from large predatory fishes in theabsence of seagrasses. Our results also suggest that marshdetritus, by providing habitat for epifauna and helping main-tain prey availability, may further temper reductions inseagrass-associated fishes and macroinvertebrates followingseagrass decline. The results highlight the importance of
marsh-bordered, shallow lagoons as habitat for small fishand macroinvertebrates regardless of seagrass cover. Thisstudy contributes to the characterization of habitat redundancyin coastal ecosystems and pinpoints the importance of consid-ering all habitats in concert for the proper understanding andmanagement of coastal ecosystems.
Keywords Coastal lagoons . Seagrass . Nekton . Epifauna .
Fringingmarsh . Gulf ofMexico
Introduction
Lagoons occupy approximately 13 % of coastlines world-wide, with the largest extent along the Atlantic and Gulf coastsof the USA, where they cover approximately 2800 km ofshoreline (Kennish and Paerl 2010). Lagoons are oftenprotected by a barrier island, spit, reef, or sand bank and con-nected to the open ocean by tidal inlets. Coastal lagoons arealso characterized by shallow waters that generally averageless than 2 m in depth, although channels and relict holesmay be deeper. Unlike estuaries, coastal lagoons do not nor-mally feature riverine inputs and freshwater mainly enters thelagoon via surface runoff and groundwater (Lehrter andCebrian 2010).
Seagrass meadows are ubiquitous in shallow coastal wa-ters, including lagoons, and function as critical habitat formany finfish and shellfish species (Beck et al. 2001; Williamsand Heck 2001). The faunal assemblages that inhabit seagrassbeds have been well documented and include both residentand transient species. Many transient species have complexlife cycles and are seasonal recruits, the majority of which arejuvenile fish and decapod crustaceans that later migrate off-shore or to other habitats where they become adults (Hecket al. 2008). In coastal waters of the northern Gulf of Mexico,
Communicated by Karin E. Limburg
Electronic supplementary material The online version of this article(doi:10.1007/s12237-015-0031-7) contains supplementary material,which is available to authorized users.
* Rachel B. [email protected]
1 Dauphin Island Sea Lab, Dauphin Island, AL, USA2 Department of Marine Sciences, University of South Alabama,
Mobile, AL, USA
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examples of resident species include rainwater killifish (Luca-nia parva), blue crab (Callinectes sapidus), and grass shrimp(Palaemonetes pugio) (Jordan 2002; Thomas et al. 1990;Welsh 1975), and transient species include pinfish (Lagodonrhomboides), red drum (Sciaenops ocellatus) and penaeidshrimp species (Farfantepenaeus aztecus and Litopenaeussetiferus) (Minello and Zimmerman 1983; Nelson et al.2013; Phillips et al. 1989; Rooker and Holt 1997).
Seagrasses have been declining worldwide due to naturaland anthropogenic processes (Waycott et al. 2009). Naturalevents include waves and storms, while anthropogenic factorsinclude dredging, harbor construction, pollution, disease, andvessel damage (Orth et al. 2006; Short and Wyllie-Echeverria1996). Although seagrass beds naturally occur as vegetatedpatches interspersed with bare sediment, anthropogenic dam-age has further fragmented seagrass beds, increasing the areaof bare sediment in coastal waters (Johnson and Heck 2006).A decline in seagrass beds may therefore negatively impactspecies that inhabit the beds and require this habitat for growthand survival, such as the resident and transient species men-tioned previously (Cebrian et al. 2009a; Hughes et al. 2009).
Fringing marsh is also a ubiquitous component of coastallagoons, and there may be significant habitat complementaritybetween seagrass beds and fringing marshes in coastallagoons. Rozas and Minello (1998) found that seagrassmeadows could provide an alternative habitat at low tide formarsh species when the marsh platform was not accessible.Similarly, seagrass-associated nekton can access fringingmarsh vegetation for food and refuge at high tide while themarsh platform is flooded (Minello et al. 2012; Moody et al.2013a; Rozas et al. 2012). Therefore, habitat complementaritybetween seagrass beds and surrounding fringing marsh couldmitigate reductions in fish habitat following declines inseagrass abundance.
Many species that frequent coastal lagoons are not com-mon in seagrass beds. For instance, Hughes et al. (2002) foundthat fish assemblages differed substantially between seagrassand bare bottom sites in New England coastal lagoons, withbenthic species such as oyster toadfish (Opsanus tau), mum-michog (Fundulus heteroclites), and grubby sculpin(Myoxocephalus anaeus) being the most abundant in seagrasssites, and pelagic schooling species such as bay anchovy(Anchoa mitchilli), Atlantic silverside (Menidia menidia),and scup (Stenotomus chrysops) being dominant in bare sed-iment sites. Minello et al. (2003) found that pinfish were moreassociated with vegetated areas whereas gulf menhaden(Brevoortia patronus), spot (Leiostomus xanthurus), andspotfin mojarra (Eucinostomus argenteus) were more as-sociated with non-vegetated areas. Therefore, speciesthat are not seagrass-associated may be minimally af-fected by seagrass loss in coastal habitats and may be-come the dominant species of the community followingseagrass loss.
The response of fish communities to varying seagrass cov-er in shallow coastal lagoons has not been as well studied as inother coastal systems that typically have greater depths, suchas bays and estuaries (Able et al. 2011; Heck et al. 1989;Hughes et al. 2002; Valesini et al. 2004). We hypothesizedthat seagrass-associated fish and macroinvertebrate speciesmay not always endure large declines with reduced seagrasshabitat in shallow lagoons surrounded by fringing marsh asthe fringing marsh may provide habitat redundancy and com-pensate for seagrass loss. In addition, extreme shallowness inthe lagoons may limit access by large fish, which would offeradditional protection to small fishes (Rozas and Minello1998). To test this hypothesis, we compared the abundanceand species composition of fish, macroinvertebrates, and epi-faunal organisms over 2 years in six extremely shallow la-goons located in the northern Gulf of Mexico that were bor-dered with fringingmarsh and had varying degrees of seagrasscover.
Methods
Study Sites
We selected six shallow lagoons with varying seagrass cover(Spanish Cove, Langley Point, State Park, Kee’s Bayou, Joe’sSite and Gongora) in Big Lagoon (Florida, USA).Within eachlagoon, we selected a sampling area that was representative ofthe entire lagoon (Fig. 1). The only exception was Kee’s Bay-ou, where we selected the vegetated north-western part of thelagoon 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 thesampling area. On each sampling date, we took eightcores haphazardly within each sampling area along withthe seine and suction samples (see below) and calculat-ed the percent of cores that had seagrass. The meanpercent of cores with seagrass for the entire study du-ration ranged from 0 to 97.3 % across lagoons(Table 1). The two easternmost lagoons, Spanish Coveand Langley Point, are dominated by turtlegrass(Thalassia testudinum) with interspersed patches ofshoalgrass (Halodule wrightii). State Park and Joe’s Sitefeatures H. wrightii as the dominant species with inter-spersed patches of widgeon grass (Ruppia maritima),whereas Kee’s Bayou has a higher abundance ofR. maritima than H. wrightii. A large fraction of theshoreline in the lagoons is bordered with fringingsaltmarsh (Table 1). In all lagoons, the fringingsa l tmarsh had a band of cordgrass (Spar t inaalterniflora) at the waterfront edge and a strip of blackneedlerush (Juncus roemerianus) landward of thecordgrass.
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Variables Measured
The study was carried out from April 2010 to January 2012.Sampling was conducted every other month from April toOctober with additional sampling in January. In shallow coast-al lagoons of the northern Gulf of Mexico, most juvenile re-cruitment occurs in winter/early spring. Juveniles remain inthe lagoons through spring and summer, and the majoritymigrate offshore with the arrival of cold fronts in fall (Cebrianet al. 2009a; Middaugh and Hemmer 1992; Nelson 2002).Therefore, this sampling timeline allowed us to capture themagnitude of winter/spring recruitment and fall migration.
Environmental Measurements
We measured water-column depth, temperature, salinity, anddissolved oxygen concentration. These measurements weretaken at three haphazardly selected locations within the sam-pling area of each lagoon on each sampling date. Depth wasmeasured with a meter stick, and temperature, salinity, and
dissolved oxygen were measured at the mid-water-columnwith a hand-held YSI 85.
Seining
Fish and large macroinvertebrates were collected using a6.0 m × 1.5 m bag seine with 3 mm mesh. Three haphazardlylocated seines were pulled for 20 m within the sampling areaof the lagoon on each collection date. A core (15.5 cm diam-eter) was taken at the center of the seine transect to assessseagrass cover in the sampling area (Table 1). The seine sam-ples were taken to the laboratory for processing. All fish andmacroinvertebrates were identified and counted. Fish weremeasured for standard and total length, and macroinverte-brates were measured from rostrum to telson (e.g., penaeidshrimp) or across the carapace (e.g., crabs). Due to overlap-ping spawning seasons and the timing of molting, it is likelythat we misidentified a few white shrimp (L. setiferus) asbrown shrimp (F. aztecus) and the two species were thereforegrouped as penaeid shrimp.
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, andSpanish Cove. Yellow lines delineate the areas sampled within the lagoons
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Suction Sampling
Epifaunal invertebrates were collected using a suctionsampler following specifications for shallow systems(Heck et al. 2001). Five samples were collected haphaz-ardly within the sampling area of the lagoon on eachsampling date. Briefly, samples were taken by placingan open ended cylinder (1.6 m high, 52.1 cm wide) ontothe sediment and creating a tight seal by pressing thecylinder into the sediment. Care was taken not to disturbthe sampling area prior to cylinder placement. Subse-quently, the epifauna enclosed within the cylinder wassuctioned out and collected with a 0.5 mm mesh bag.The area enclosed by the cylinder was swept with a handnet after suctioning to ensure that most epifauna werecollected. In addition, we collected a core (15.5 cm di-ameter) haphazardly around the cylinder margin to deter-mine seagrass cover in the sampling area (Table 1).
The samples were transported to the laboratory on ice andfrozen for later examination. Upon thawing, the samples weredyed with Rose Bengal and separated into major taxonomicgroups for identification and abundance counts. The groupswere amphipod, isopod, gastropod, mysid, paguridae, tanaid,echinoderm, Bshrimp^ (penaeid, alpheidae, and othercarideans), and Bcrab^ (xanthidae and portunidae).
Clipping Experiment
Our hypothesis was that, in shallow coastal lagoonssurrounded with fringing marsh, the abundance of seagrass-associated fish and macroinvertebrate species would not dras-tically be reduced with decreased seagrass cover due to habitatcomplementarity offered by the fringing marsh. Seagrass de-cline should cause the loss of refuge and food (i.e., epiphytesand epifauna) for seagrass-associated species but, if fringingmarshes offset that loss due to habitat complementarity, thenwe should not find large decreases in the abundance ofseagrass-associated species. To test this hypothesis, we havemeasured both the abundance of seagrass-associated fish,large macroinvertebrates, and epifauna in lagoons with vary-ing seagrass cover. We expect large reductions in epifaunalabundance with decreased seagrass cover, but not necessarilyin fish and large macroinvertebrate abundance. In addition, tofurther test how epifauna abundance changes with reducedseagrass cover, we carried out a clipping experiment in thelagoon 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 m2
plots located within the lagoon sampling area were clippedwith scissors at the base of the leaves. One day after clipping,suction sampling was carried out in the clipped plots and invegetated areas haphazardly located in the lagoon as describedabove. To account for edge effects, the size of the trimmedT
able1
Environmentaldata,seagrasscoverandfractio
nof
lagoon
perimeterbordered
with
fringing
marsh.P
ercentcoveriscalculated
asthepercentoftheeightcores
takenon
each
samplingdatethat
hadseagrass
(see
BStudy
Sites^).Environmentald
ataencompass
allsam
plingdatesexcept
April2010
fordissolvedoxygen,salinity,and
temperature
Dissolved
oxygen
Salinity
Temperature
Dept(m)
mg/L
%ppt
°CPercentcores
with
seagrass
Perimeter
ofthesampled
area
(m)
Marsh
border
(m)
Fractio
nof
perimeter
bordered
bymarsh
Site
Range
Mean(±SE
)Range
Mean(±SE
)Range
Mean(±SE
)Range
Mean(±SE
)Range
Mean(±SE
)Range
Mean(±SE
)
SpanishCove
0.35–0.880
58(±0.0)
8.1–13.3
10.2(±0.6)
120.5–202.1
143.6(±9.1)
23.7–34.4
27.6(±1.1)
14.4–33.1
25.3(±2.4)
75.0–100.0
97.5(±2.5)
642
336
0.52
Kee’sBayou
0.41–0.80
0.60
(±0.05)
5.3–9.7
7.5(±0.6)
67.9–142.5
103.7(±8.0)
13.4–26.2
20.6(±1.3)
15.3–34.1
26.6(±2.2)
75.0–100.0
92.5(±2.8)
537
362
0.67
StatePark
0.29–0.86
0.54
(±0.05)
7.7–10.0
9.2(±0.3)
103.8–158.0
123.7(±7.2)
20.2–28.9
23.6(±1.0)
14.1–34.6
25.5(±2.4)
50.0–100.0
85.0(±5.8)
502
222
0.44
Langley
Point
0.24–0.81
0.61
(±0.06)
5.1–10.1
7.9(±0.6)
76.4–151.5
105.9(±8.2)
20.7–29.3
25.0(±0.9)
16.5–33.7
25.3(±2.1)
50.0–100.0
83.8(±4.9)
782
648
0.83
Joe’sSite
0.35–0.85
0.57
(±0.06)
5.6–10.8
8.5(±0.7)
82.2–168.2
113.0(±9.2)
19.9–30.3
24.1(±1.1)
13.2–34.0
25.6(±2.2)
0.0–50.0
18.8(±5.7)
329
173.2
0.53
Gongora
0.58–0.98
0.80
(±0.05)
4.2–10.4
7.6(±0.6)
64.1–140.5
101.5(±7.7)
20.7–27.8
23.8(±0.8)
12.9–32.6
26.2(±2.2)
00
852
345.5
0.41
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plots was 50 cm larger than the diameter of the suction sam-pling cylinder. Samples from the trimmed plots were proc-essed in the same fashion as samples from the adjacent vege-tated areas (see 2.2c BSuction Sampling^). We also comparedepifaunal abundance in the clipped plots (which still had thebase of the shoots present) with the abundance measured inGongora, the lagoon with no seagrass, to gain further insightof how reduced structure affects epifaunal abundance.
Statistical Analyses
Abundance data for fish, large macroinvertebrates, and epi-fauna were analyzed using a mixed two-way analysis of var-iance (ANOVA) with Blagoon^ as a fixed factor andBsampling time^ as a random factor. If lagoon was significantin the two-way ANOVA and both sampling time and the in-teraction between lagoon and sampling time were not, sam-pling times were pooled for each lagoon and the lagoons com-pared with one-way ANOVA followed by Tukey tests. If theinteraction was significant regardless of whether lagoon orsampling time were significant or not, or if lagoon and sam-pling time were significant and the interaction was not, one-way ANOVA and Tukey comparisons among lagoons weredone separately for each sampling time (Quinn and Keough2002). Abundances were square root transformed to complywith the assumptions of ANOVA. Despite the square roottransformation, ANOVA assumptions were not fully met insome cases and theα value was lowered to 0.001 to reduce thechances of committing type I error.
To examine whether differences in fish and macroinverte-brate individual size existed across lagoons, we compared ourindividual length measurements among lagoons for each sam-pling date with a one-way ANOVA followed by Tukey tests.Comparisons among lagoons were done for each samplingdate separately as most species had sampling dates wherewe captured no individuals in some lagoons. Length data weresquare root transformed and the α value lowered to 0.001.ANOVA was conducted using the Minitab 14 statisticalsoftware.
Seining is regarded as an adequate technique to capturemacroinvertebrates and small individuals of fish species asso-ciated with seagrass structure (Rozas and Minello 1997,1998). However, seining may not adequately sample pelagicschooling species, such as gulf menhaden and bay anchovy(Rozas and Minello 1997); therefore, we did not considerthose species in our analysis. Furthermore, we only collectedthree 6.0 m × 1.5 m bag seines at each lagoon on each sam-pling time, with each seine covering a 20 m transect; thissampling effort may have been too low for non-abundant spe-cies (Cebrian et al. 2009a). Therefore, we focused our analy-ses on ten abundant seagrass-associated species of fish andmacroinvertebrates that are considered to be adequately sam-pled with seining. These species allow for a strong test of how
seagrass-associated species respond to decreasing seagrasscover in shallow coastal lagoons surrounded with fringingmarsh and whether there is evidence of habitat complemen-tarity between seagrass beds and adjacent fringing marshes.
Results
Environmental Measurements
Mean depth was <1m in the areas sampled within the lagoons.The areas ranged widely in seagrass cover (Table 1), with fourlagoons (Spanish Cove, Kee’s Bayou, State Park, and LangleyPoint) having high seagrass cover (83.8–97.5 %), one (Joe’ssite) having low cover (18.8 %), and one (Gongora) having noseagrass. Water temperature reflected typical seasonal vari-ability, with values ranging from ca. 13 to 35 °C. Salinityvalues varied between mesohaline and euhaline conditions,as typically found in Big Lagoon (Stutes et al. 2007). Ourmeasurements of oxygen concentration during daytimereflected well-oxygenated waters. Mean values of oxygenconcentration, salinity, and temperature were similar amongthe lagoons.
Fish and Macroinvertebrate Abundance
A diverse assemblage of fish and macroinvertebratestotaling 108,234 individuals was collected during thisstudy. We captured 55 species of fish and 8 taxa (identifiedto genus or species level) of macroinvertebrates (ElectronicSupplementary Material 11). We focused our analyses on tenseagrass-associated species or taxa that are adequately cap-tured with seining (see 2.3 BStatistical Analyses^). These spe-cies are grass shrimp, pinfish, rainwater killifish (Lucaniaparva), penaeid shrimp, blue crab, inland silverside (Menidiaberyllina), clown goby (Microgobius gulosus), spotfinmojarra, code goby (Gobiosoma robustum), and darter goby(Ctenogobius boleosoma) (Table 2). We also included spot(Leiostomus xanthurus), a non seagrass-associated speciescaptured in high abundance.
We did not find a strong tendency for seagrass-associatedspecies to have higher abundances in the highly seagrass-vegetated 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 samplingtime for grass shrimp, pinfish, rainwater killifish, penaeidshrimp, inland silverside, clown goby and code goby. For bluecrabs, both main time and lagoon effects were significant, butthe interaction was not. When lagoons were compared separate-ly for each sampling date for each of these species, we found acommon outcome; significant differences were not foundamong the lagoons on most dates, and when we did, severalof the highly vegetated lagoons did not have significantly higher
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Tab
le2
Speciesanalyzed.T
otalcountsforalllagoons
andallsam
plingdatesareprovided.Informationon
theirlifehistory(spawning,recruitm
ent,andmovem
ent)isalso
provided
Species
nSpawning
Recruitm
ent
Movem
ent
Literature
Grass
shrimp(Palaemonetes
pugio)
49,236
Latespring
throughfall
Resident
Annualspecies
(13month
lifespan)
Anderson1985;W
elsh
1975
Pinfish(Lagodon
rhom
boides)
18,125
Latefallto
earlyspring
offshore
(som
emay
occurinshore)
Juvenilesenterestuarieslate
winterthroughspring
Migrateouto
festuarieslatefall
Muncy
1984;N
elson2002
Rainw
ater
killifish
(Lucania
parva)
8141
Early
summer
Resident
Migrateto
freshwater
tobreed
Moyle1976;Jordan2002
Penaeid
shrimp(Farfantepenaeus
aztecusandLitopenaeussetiferus)
4152
OffshoreF.aztecus:Septem
ber–May,
butcan
occuryear
roundL.
setiferus:A
pril-October
Estuarine
recruitm
entb
egins
2–3weeks
afterspaw
ning
Bothspeciesmigrateatmaturity
from
winter-spring
F.aztecus
migratesoffshore
L.setiferus
migratesto
nearshorewaters
Lassuy1983;L
indner
and
Anderson1956;M
inello
andZim
merman
1983
Bluecrab
(Callin
ectessapidus)
2959
Estuarine
andcoastalo
ccurs
spring
throughsummer
Estuarine
recruitm
ento
ccurs
from
summer
toearlywinter
Females
migratedownestuaryin
fall;
juvenilesandmales
move
into
deeper
water
overwinter
Hines
andRuiz1995;H
ines
2007;P
erry
andMcIlwain
1986;T
homas
etal.1990;
Murphyetal.2007
Inland
silverside
(Menidia
beryllina)
1607
Spring
inupperestuary
YOYfoundin
upperestuary
during
summer
Migrateto
lower
estuaryin
fallat
35–45mm
Gleason
andBengtson1996
Clowngoby
(Microgobius
gulosus)
1064
Spring
tolatefall
Resident
Nomigratio
n;adultsburrow
over
winter
Gaisner2005
Spotfinmojarra
(Eucinostomus
argenteus)
982
Suggestedto
beduring
the
warmer
months
Juvenilesfoundin
lagoonsand
inshoreareasseasonally
Foundin
oraround
inletsin
warmer
months
Kerschner
etal.1985;
Livingston
1984;R
ichards2004
Codegoby
(Gobiosomarobustum
)695
Latespring
toearlysummer
andlatesummer
toearly
fall
Resident
Nomigratio
n;annualfish
(1-year
lifespan)
Springer
andMcE
rlean1961
Dartergoby
(Ctenogobius
boleosom
a)661
Suggestedto
peak
inmid
summer
Resident
Nomigratio
nHendonetal.2
001;
Hildebrand
andCable1938
Spot
(Leiostomus
xanthurus)
12,339
Offshorefrom
fallto
earlyspring
Winterthroughearlyspring
Falloffshore
migratio
nforspaw
ning
BoeschandTurner1984;P
hillips
etal.1989
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abundances than the sparsely vegetated lagoons. For spotfinmojarra, we did not find any significant differences amonglagoons on any sampling date. Dates were pooled for thecomparison across lagoons for darter goby since both the maintime effect and the interaction were not significant. For thisspecies, we also found that several highly vegetated lagoonsdid not significantly have higher abundance than the sparselyvegetated lagoons. The abundance of spot, a species with littleassociation to seagrasses, varied over time but not acrosslagoons (Table 3; Electronic Supplementary Material 10).
Fish and Macroinvertebrate Size
We did not find clear and consistent differences in individualsize between high and low seagrass-vegetated lagoons for thefish and macroinvertebrate species examined. Pinfish tendedto be larger in Gongora (no seagrass cover) than most otherlagoons during summer and fall (Table 4; Fig. 3a). The size ofrainwater killifish was often larger in Spanish Cove (ahighly vegetated lagoon) in relation to other lagoons(Table 4; Fig. 3b).
For most species, size histograms reflected the temporaldynamics of recruitment and growth through the year. Pinfishwere smallest in January and generally increased in size dur-ing 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, Augustand January (Fig. 3b). For penaeid shrimp, however, no con-sistent differences in size were found through time (ElectronicSupplementary Material 11). Blue crabs were smallest in Jan-uary, although many small blue crabs were also found in othermonths, and large adults were mainly found in summer(Electronic Supplementary Material 12). No clear temporalpattern was evident for the size of inland silversides, although
numerous small fish were found in some lagoons in January(Electronic Supplementary Material 13). Small clown gobieswere mainly found in June and October (ElectronicSupplementary Material 14). Spotfin mojarra displayed boththe smallest and largest individuals in August and October,with intermediate sizes in the other months (ElectronicSupplementary Material 15). Code gobies were generallysmallest in October and January and largest in April and June(Electronic Supplementary Material 16). We generally foundlarger darter gobies in June and smaller ones in January duringthe first year of the study (Electronic Supplementary Material17). Spot were smallest in January and grew over time to reachmaximum values in fall (Electronic SupplementaryMaterial 18).
Table 3 ANOVA results for fish and macroinvertebrate abundance.Results from Tukey analyses are depicted in Fig. 2 as pertinent (see text)
Datep value
Lagoonp value
D × Lp value
Grass shrimp 0.273 ≤0.001 ≤0.001Pinfish ≤0.001 ≤0.001 ≤0.001Rainwater killifish 0.034 ≤0.001 ≤0.001Penaeid shrimp 0.166 0.003 ≤0.001Blue crab ≤0.001 ≤0.001 0.117
Inland silverside 0.013 0.013 ≤0.001Clown goby 0.009 ≤0.001 ≤0.001Spotfin mojarra 0.005 0.352 0.007
Code goby ≤0.001 ≤0.001 ≤0.001Darter goby 0.002 ≤0.001 0.013
Spot ≤0.001 0.002 0.002
Fig. 2 Abundance (individuals per square meter) of abundant species ofseagrass-associated macroinvertebrates and small fish. a grass shrimp; bpinfish. Before plotting, 1 was added to each abundance value and thissum was log transformed. Plotted values denote the mean for each lagoonand sampling date, and the line on the values denotes ± SE. Tukey com-parisons among lagoons are shown as pertinent (i.e., for each samplingdate separately or pooling all dates together, see text). Green symbolscorrespond to highly vegetated lagoons, and orange symbols to sparselyvegetated lagoons (see text): S Spanish Cove, K Kee’s Bayou, P StatePark, L Langley Point, J Joe’s Site, G Gongora, ns non-significant
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Epifaunal Abundance
All nine epifaunal groups displayed a significant interactionbetween lagoon and sampling time (Fig. 4a, b; ElectronicSupplementary Material 19–25; Table 5). When abundancewas compared among lagoons separately for each samplingdate, we found significant differences on one out of ten sam-pling dates for crabs and mysids (Electronic SupplementaryMaterial 21, 24); three dates for echinoderms (ElectronicSupplementary Material 25); four dates for amphipods andisopods (Fig. 4a, b); five dates for paguridae and tanaids(Electronic Supplementary Material 22, 23); six dates forshrimp (Electronic Supplementary Material 19); and eightdates for gastropods (Electronic Supplementary Material 20).The sum of the abundance of all nine groups displayed signif-icant differences among the lagoons on seven sampling dates(Electronic Supplementary Material 26). For all samplingdates where significant differences were found among la-goons, several highly seagrass-vegetated lagoons did not havehigher abundances than the sparsely vegetated lagoons(Fig. 4a, b; Electronic Supplementary Material 19–26).
Clipping Experiment
We found reduced epifaunal abundance in clipped comparedto non-clipped plots in Spanish Cove on three out of the foursampling dates (Fig. 5). We found reduced epifaunal abun-dance in Gongora in relation to clipped plots in Spanish Covein two out of the four sampling dates (Fig. 5).
Discussion
This study examines the abundance of ten seagrass-associatedspecies of macroinvertebrates and small fish in six extremely
shallow coastal lagoons (mean depth < 1 m) in the northernGulf of Mexico. The areas sampled in the lagoons featuredcontrasting levels of seagrass cover, with four having highcover (83.8–97.5 %) and two having no or low cover (0–18.8 %), but all of them surrounded in part with fringingmarsh. Our hypothesis was that the abundance of these specieswould not consistently and largely be reduced in low vegetat-ed in relation to high vegetated lagoons owing to habitat re-dundancy provided by the surrounding marsh and additionalprotection against large fish offered by their extreme shallow-ness (Minello et al. 2012; Moody et al. 2013a; Rozas andMinello 1998; Rozas et al. 2012). Our results support thishypothesis. For all those species, we found no significant dif-ferences in abundance among the lagoons on most samplingdates and, when we did, several highly vegetated lagoons didhave larger abundances than sparsely vegetated lagoons.Thus, the ten seagrass-associated species studied here wereoften as abundant in low vegetated lagoons as they were inhigh vegetated lagoons. The abundance of spot, a nonseagrass-associated species, did not vary across lagoons.
The type of dominant seagrass did not seem to affect ourconclusion. Spanish Cove and Langley Point had mostlyturtlegrass and some patches of shoalgrass. Shoalgrass wasdominant in State Park and Joe’s site, where some widgeongrass also occurred. Widgeon grass was dominant in Kee’sBayou, where some shoalgrass also occured. Thus, sparselyvegetated lagoons often had similar abundances of seagrass-associated fish and macroinvertebrates as did highly vegetated
Table 4 ANOVA results for individual fish length. Lagoons arecompared for each sampling date. Corresponding Tukey comparisonsare depicted in Fig. 3 and ESM 2–9. In a few cases (i.e., blue crab inJanuary 2011 and October 2011; clown goby in April 2010; and darter
goby in April 2010 and October 2010), we did not find significant pair-wise differences with the Tukey comparisons despite obtaining a signif-icant one-way ANOVA. na not applicable (we did not capture two ormore individuals in at least two of the lagoons on the given date)
April2010
June2010
August2010
October2010
January2011
April2011
June2011
August2011
October2011
January2012
Pinfish ≤0.001 ≤0.001 ≤0.001 ≤0.001 ≤0.001 ≤0.001 ≤0.001 ≤0.001 ≤0.001 0.073
Rainwater killifish ≤0.001 ≤0.001 ≤0.001 ≤0.001 ≤0.001 ≤0.001 ≤0.001 ≤0.001 ≤0.001 ≤0.001Penaeid shrimp ≤0.001 ≤0.001 ≤0.001 ≤0.001 0.515 0.007 ≤0.001 ≤0.001 ≤0.001 ≤0.001Blue crab ≤0.001 0.007 0.428 0.210 ≤0.001 ≤0.001 0.772 0.104 ≤0.001 ≤0.001Inland silverside ≤0.001 ≤0.001 0.089 ≤0.001 ≤0.001 ≤0.001 ≤0.001 ≤0.001 ≤0.001 0.093
Clown goby ≤0.001 ≤0.001 n.a ≤0.001 0.740 0.002 ≤0.001 ≤0.001 0.138 0.019
Spotfin mojarra n.a. n.a. 0.007 ≤0.001 0.004 n.a. n.a. ≤0.001 ≤0.001 n.a.
Code goby 0.019 0.400 n.a. n.a. 0.202 0.764 ≤0.001 0.604 ≤0.001 ≤0.001Darter goby ≤0.001 0.205 0.033 ≤0.001 0.616 0.029 n.a. n.a. 0.106 0.153
Spot ≤0.001 ≤0.001 0.005 0.231 ≤0.001 ≤0.001 ≤0.001 ≤0.001 0.736 ≤0.001
�Fig. 3 Individual length histograms. a pinfish; b rainwater killifish.Values on the y-axis denote the percent of individuals captured, andvalues on the x-axis correspond to length expressed in mm. Tukeycomparisons among lagoons are shown above corresponding samplingdates (see Table 4). Symbols as in Fig. 2. ns non-significant, na notapplicable (we did not capture two or more individuals in at least twoof the lagoons on the given date)
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lagoons regardless of the dominant seagrass species in thehighly vegetated lagoon. Previous research has found thatdifferences in structural complexity among seagrass speciesmay lead to differences in the abundance and type of associ-ated fauna (Boström et al. 2006; Connolly and Hindell 2006),but here, we do not find large and consistent differences inseagrass-associated fauna density among highly vegetated la-goons dominated by different seagrass species or betweenthose lagoons and low vegetated (including one lagoon withno seagrass) lagoons. Our findings should not be affected bylagoon accessibility to new fish andmacroinvertebrate recruitssince all lagoons have well connected mouths to the samelarge body of water, Big Lagoon, which in turn is connectedwith a wide passage to the open waters of the Gulf of Mexico.
The lagoons studied here are partly bordered by fringingmarsh, and it is well known that fringing marsh constituteshabitat for many species of fish and macroinvertebrates
(Boesch and Turner 1984; Irlandi and Crawford 1997;Minello et al. 2012). In particular, the transitional slope be-tween the seaward limit of the marsh and open water of thelagoon is a Bhotspot^ used by many fish and macroinverte-brates for refuge and food, including the species considered inthis study (Moody et al. 2013a; Rozas and Minello 1998;Stunz et al. 2010). Themarsh may also transition into lagoonalopen water as a steep escarpment, which features high levelsof structural complexity that can provide shelter for numerousorganisms (Boesch and Turner 1984; Minello et al. 2003;Moody et al. 2013b). In addition, the marsh platform can alsobecome habitat for many fish and macroinvertebrates when
Fig. 4 Abundance of epifauna captured with suction sampling. aamphipods; b isopods. Before plotting, 1 was added to each abundancevalue and this sum was log transformed. Plotted values denote the meanfor each lagoon and sampling date, and the line on the values denotes ±SE. Tukey comparisons among lagoons are shown for each sampling dateseparately (see text). Symbols as in Fig. 2. ns non-significant
Table 5 ANOVA results for epifauna abundance. Results from Tukeyanalyses are depicted in Fig. 4 as pertinent (see text)
Datep value
Lagoonp value
D × Lp value
Amphipod ≤0.001 ≤0.001 ≤0.001Isopod 0.024 ≤0.001 ≤0.001Shrimp 0.092 ≤0.001 ≤0.001Gastropod 0.080 ≤0.001 ≤0.001Crabs 0.079 ≤0.001 ≤0.001Paguridae 0.631 ≤0.001 ≤0.001Tanaid ≤0.001 ≤0.001 ≤0.001Mysid ≤0.001 0.010 ≤0.001Echinoderm 0.041 ≤0.001 ≤0.001Total 0.112 ≤0.001 ≤0.001
Fig. 5 Total epifaunal abundance (sum of the nine groups shown inFig. 4) in non-clipped and clipped plots in Spanish Cove and inGongora. Bars correspond to mean values and lines to ± SE.Abundance was compared between non-clipped and clipped plots, andbetween clipped plots and Gongora for each time separately with a t test.Data were square root transformed and met the conditions of normalityand homocedasticity. Asterisks denote significant differences at p ≤ 0.05
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flooded at high tides. For instance, blue crabs, penaeid shrimp,grass shrimp, pinfish, darter goby, rainwater killifish, and in-land silverside may dwell on the marsh platform when it issubmerged at high tide (Peterson and Turner 1994; Rozas andMinello 1998). Indeed, prior work has indicated that fringingmarshes can act as redundant habitats to seagrass beds(Minello et al. 2012; Rozas and Minello 1998; Rozaset al. 2012).
The extreme shallowness of the lagoons studied may con-stitute another mechanism by which these lagoons providerefuge regardless of the amount of seagrass cover. We nevermeasured water depths greater than 1 m in any of the lagoons,although depths greater than 1 m are possible on extremelyhigh tides (Cebrian et al. 2009a). Measured depths rangedfrom 24 to 98 cm, and mean depths were ≤80 cm. Such shal-low conditions could significantly restrict access by largepredatory fish, thereby providing protection to macroinverte-brates and small fish. Accordingly, it has been shown thatpredation risk for small fish increases with depth (Hines andRuiz 1995; Rozas and Minello 1998; Ruiz et al. 1993).
Unlike the ten seagrass-associated species of fish and mac-roinvertebrates studied, we expected a decrease in epifaunalabundance with reduced seagrass abundance. The clippingexperiment in Spanish Cove, a highly vegetated lagoon, didshow lower epifaunal abundance in clipped compared to non-clipped plots on three out of the four dates the experiment wascarried out. However, the results from the epifaunal abun-dance survey in the lagoons were somewhat equivocal. Outof our ten sampling dates, we found differences in abundanceamong lagoons on one date for crabs and mysids, three datesfor echinoderms, four dates for amphipods and isopods, fivedates for paguridae and tanaids, six dates for shrimp, and eightdates for gastropods. Furthermore, several highly vegetatedlagoons did not have larger abundances than sparselyvegetated lagoons on the dates where we found differ-ences among lagoons. Overall, these results indicatemany instances during our 2-year survey where theabundance of these epifaunal groups was not higher inhighly vegetated than in sparsely vegetated lagoons, de-spite the large differences in seagrass cover that existedbetween these two groups of lagoons.
While the reasons remain unclear, we suggest the lack oflarge and consistent differences in epifaunal abundance withreduced seagrass cover among the lagoons compared to bepartially explained by marsh detritus that falls onto the bottomof the lagoons. Marsh detritus is a common feature on thebottom of the lagoons studied (Cebrian et al. 2009b; Ferrero-Vicente et al. 2011; Stutes et al. 2007), and the debris may behabitat for epifaunal organisms particularly in lagoons withlittle or no seagrass. The comparison between Gongora, alagoon without seagrass, and clipped plots in Spanish Cove,offers support to this suggestion. Clipped plots were left withthe base of the seagrass shoots, which still provided some
structure for epifauna. Out of the four dates compared, epifau-nal abundance was higher in the clipped plots in Spanish Covethan in Gongora on two dates but not on the other two dates.By providing habitat for epifauna, the occurrence of marshdetrital debris in Gongora may help explain why epifaunaabundance did not differ between this lagoon and the clippedplots in Spanish Cove on half of the dates compared. In addi-tion, marsh detrital debris, through helping maintain preyavailability, may help temper declines in seagrass-associated fish and macroinvertebrates followingseagrass decline.
We did not find any consistent differences in individualsize of the seagrass-associated fish and macroinvertebratesstudied between highly and sparsely seagrass-vegetated la-goons. In general, temporal changes in the size distributionof the species studied reflected its life history and patterns ofrecruitment and movement in coastal systems. In what fol-lows, we discuss a few examples. The mean size of pinfishwas smallest in January and increased through spring, sum-mer, and fall, consistent with their recruitment to coastal sys-tems in winter, residence through spring and summer, andmigration offshore in fall (Cebrian et al. 2009a; Nelson et al.2013). We observed large abundances of small blue crabs inJanuary, consistent with the majority of recruitment occurringin summer to late fall (Hines 2007; Murphy et al. 2007; Thom-as et al. 1990), and large individuals in summer, consistentwith spawning seasons from spring to fall and the migrationof larger juveniles and adults to deeper waters in fall/earlywinter (Hines and Ruiz 1995; Perry and McIlwain 1986).Code gobies were largest in spring and summer, and smallestin fall and winter, consistent with a spawning period from latespring to early fall and their annual life cycle (Springer andMcErlean 1961). Similar to pinfish, spot was smallest in Jan-uary and increased in mean size through spring and summer toreach maximum size in fall, which is consistent with theirrecruitment to coastal waters in winter, residence throughoutthe spring and summer, and migration offshore in fall as tem-perature drops (Phillips et al. 1989).
In conclusion, our study provides evidence of habitat re-dundancy between seagrass beds and fringing marshes forseagrass-associated species of fish and macroinvertebrates inshallow coastal lagoons. Such redundancymay partially offsetdeclines of these species following seagrass loss. Extremeshallowness may also contribute to providing refuge fromlarge predators in the absence of seagrasses. Marsh detritaldebris, through providing habitat for epifauna and helpingmaintain prey availability, may also temper declines inseagrass-associated fish and macroinvertebrates followingseagrass decline. These results highlight the important roleof marsh-bordered, shallow lagoons as habitat for small fishand macroinvertebrates regardless of seagrass cover. Furtherstudies on extent, regulation, and implications of habitat re-dundancy in coastal ecosystems will improve our
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understanding and management capability of these importantecosystems.
Acknowledgments We would like to thank all of the technicians andinterns who assisted in the field, especially J. Goff, S. Kerner, D. Byron,W. Scheffel, C. Havard, J. Gulbranson, A. Macy, J. Reynolds, J.Hemphill, M.Metcalf, L. Schumacher, and J.McDonald.We are thankfulto Sharon Herzka for providing valuable comments on prior versions ofthe manuscript. We also thank two anonymous reviewers for their valu-able insights and improvement of themanuscript. This project was fundedby a Shelby Center Fisheries Grant.
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