Mangrove expansion into salt marshes alters associated faunal communities

Mangrove expansion into salt marshes alters associated faunal communities

Accepted Manuscript Mangrove expansion into salt marshes alters associated faunal communities Delbert L. Smee, James A. Sanchez, Meredith Diskin, Carl...

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Accepted Manuscript Mangrove expansion into salt marshes alters associated faunal communities Delbert L. Smee, James A. Sanchez, Meredith Diskin, Carl Trettin PII:

S0272-7714(17)30133-6

DOI:

10.1016/j.ecss.2017.02.005

Reference:

YECSS 5381

To appear in:

Estuarine, Coastal and Shelf Science

Received Date: 6 April 2016 Revised Date:

26 January 2017

Accepted Date: 3 February 2017

Please cite this article as: Smee, D.L., Sanchez, J.A., Diskin, M., Trettin, C., Mangrove expansion into salt marshes alters associated faunal communities, Estuarine, Coastal and Shelf Science (2017), doi: 10.1016/j.ecss.2017.02.005. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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Mangrove Expansion into Salt Marshes Alters Associated Faunal Communities

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Delbert L. Smee1*, James A. Sanchez1, Meredith Diskin1, Carl Trettin2

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*Correspondence: [email protected] ; 361.825.3637

Texas A&M University – Corpus Christi, Department of Life Sciences, 6300 Ocean Dr. Corpus Christi, TX 78412

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US Forest Service Southern Research Station, Cordesville, South Carolina 29434

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Author Contributions: DLS, JAS, and CT conceived the idea and designed the experiment. DLS and CT acquired funding. DLS, JAS, and MD collected the samples and generated the data. DLS, JAS, MD, and CT analyzed the data, and then wrote and edited the manuscript.

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Abstract

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Climate change is altering the distribution of foundation species, with potential effects on

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organisms that inhabit these environments and changes to valuable ecosystem functions. In the

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Gulf of Mexico, black mangroves (Avicennia germinans) are expanding northward into salt

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marshes dominated by Spartina alterniflora (hereafter Spartina). Salt marshes are essential

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habitats for many organisms, including ecologically and economically important species such as

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blue crabs (Callinectes sapidus) and Penaeid shrimp (e.g., Penaeus aztecus), which may be

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affected by vegetation changes. Black mangroves occupy higher tidal elevations than Spartina,

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and when mangroves become established, Spartina is replaced by mangroves at its highest

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elevations and exists only at its lowest elevations where it is bordered by mangroves. We

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compared nekton and infaunal communities within monoculture stands of Spartina that were

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bordered by mangroves to nearby areas where mangroves have not yet become established.

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Nekton and infaunal communities were significantly different in Spartina stands bordered by

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mangroves, even though salinity and temperature were not different. Overall abundance and

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biomass of nekton and infauna was significantly higher in marshes without mangroves,

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although crabs and fish were more abundant in mangrove areas. Black mangrove expansion as

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well as other ongoing vegetation shifts will continue to progress in a warming climate.

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Understanding how these changes affect species distribution and abundance are necessary for

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management, mitigation, and conservation.

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Key Words: Spartina alterniflora, Avicennia germinans, vegetation shift, climate change, shrimp

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Introduction Foundation species are critically important for the structure and function of communities and for ecosystem processes such as carbon cycling and energy flow (Ellison et al.,

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2005). Landscape level shifts in the distribution and abundance of foundation species can

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fundamentally alter ecosystems (Armitage et al., 2015), and are presently occurring with

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poleward vegetation species shifts caused by climate change (Micheli et al., 2008; Osland et al.,

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2013; Vegés et al., 2014) in both aquatic and terrestrial ecosystems (Gonzalez et al., 2010). For

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example, in North Carolina, eel grass (Zostera marina) is being displaced by shoal grass

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(Halodule wrightii), reducing biodiversity in these areas (Micheli et al., 2008). A similar

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transition is underway in Texas, where shoal grass is being displaced by the tropical seagrasses

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Syringodium filiforme (manatee grass) and Thalassia testudinum (turtle grass), significantly

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changing seagrass-associated fauna (Ray et al., 2014).

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Along the eastern and Gulf of Mexico coasts of the US, salt marshes are abundant and

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provide numerous ecosystem services including shoreline protection, carbon and nutrient

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cycling, and essential habitat for many species (Cuddington et al., 2011). At low tidal elevations,

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salt marshes are dominated by Spartina alterniflora (hereafter Spartina), an essential

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foundation species, that creates critical habitat for many ecologically and economically

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important species (e.g., blue crabs, Callinectes sapidus and red drum, Sciaenops ocellatus), and

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serves as a significant detrital input that forms the basis for coastal food webs (Rozas and

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Zimmerman 2000; Pennings and Bertness 2001; Simas et al. 2001; Stunz et al. 2002). Several

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other salt-tolerant species are present at higher tidal elevations (e.g., Spartina patens, Batis

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maritima, Salicornia virginica) and also provide habitat and shoreline protection. Primary

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production by marsh plants is critical for associated fauna, and detrital inputs can influence

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secondary production in adjacent systems (Peterson and Howarth, 1987; Pennings and

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Bertness, 2001).

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In tropical climates, Spartina is outcompeted by mangrove trees that are well adapted to coastal environments (Reef et al., 2010; Simpson et al., 2013), and mangrove forests replace

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salt marshes as the primary coastal wetland. Recent studies have documented a northward

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migration of black mangroves (Avicennia germinans), attributed to a reduction in severe

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freezing events over the past 3 decades (Cavanaugh et al., 2014). Spartina also faciliates

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mangrove expansion by trapping seedlings in suitable growth areas (Peterson and Bell, 2012)

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and by creating a warmer layer that surrounds seedlings, protecting them from cold

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temperatures (Guo et al., 2013). Historically in the Western Gulf of Mexico, particularly in

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Texas, black mangroves were present, but populations periodically expanded, displacing other

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marsh plants, and then contracted allowing those plants to reemerge in response to variations

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in climate, but black mangroves did not become established in subtropical climates that

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experienced winter freezes (Sherrod and McMillan 1981; Sherrod and C 1985; McMillan 1986;

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Cavanaugh et al. 2014). However, the frequency of severe cold weather events has declined,

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and black mangroves have migrated northward and expanded their distribution in the Gulf of

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Mexico. In the Mission-Aransas Estuary near Aransas Pass, Texas, USA, only 65 acres of black

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mangrove forest were reported in the 1980s. From 1989-2005, black mangroves expanded and

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are estimated to cover between 15,000 – 21,500 acres (Montagna et al. 2007). Expanding

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mangrove populations in Texas have displaced Spartina and other plants (e.g., S. virginica, B.

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maritima) in coastal marshes ( Everitt et al., 2010; Armitage et al., 2015).

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Salt marshes are among the most productive ecosystems on earth, and their detrital input is an important resource for many species in the marsh and in adjacent communities

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(Pennings and Bertness, 2001; Simas et al., 2001). Like marshes, mangrove forests are

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productive and support a diversity of fauna that are ecologically and economically important

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(Vaslet et al., 2012). However, there are considerable differences in the composition and

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allocation of biomass among marshes and mangroves. Standing biomass is greater in

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mangroves than marshes, while marshes tend to exhibit higher net primary productivty (Alongi,

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1998; Alongi et al., 2004). Organic matter turnover is lower in mangrove forests than marshes

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because ~ 60% of the mangrove biomass is woody (Alongi, 1998; Castañeda-Moya et al., 2013).

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Soil conditions and biogeochemical processes also differ between these habitats (Patterson and

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Mendelssohn, 1991; Perry and Mendelssohn, 2009; Comeaux et al., 2012;), however those

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differences may not be evident soon after a change in plant community composition (Henry

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and Twilley, 2013). Despite the noted differences in detrital production, biomass, and soil

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processes, few studies have assessed the impacts of mangrove encroachment into marshes on

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associated fauna, although two recent studies suggest that the effects on associated nekton

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and benthic fauna are likely to be significant (Caudill, 2005; Lunt et al., 2013).

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The northward migration of mangroves in the Gulf Coast has been occurring for the past

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25+ years and if populations continue to expand their range, replacement of Spartina as the

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primary coastal wetland species may occur (Montagna et al. 2007, Osland et al. 2013), but the

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effects on associated fauna remain obscure. Here, we measured the tidal elevation

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distributions of Spartina and black mangroves in the Western Gulf of Mexico. Then, we

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collected nekton and infaunal organisms at two tidal elevations in marshes dominated by black

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mangroves and in marshes where black mangroves were rare. These marshes were separated

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by < 10 km and had similar abiotic conditions, allowing us to assess the effects on mangrove

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encroachment on associated fauna.

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Methods

This study was performed in the Mission-Aransas National Estuarine Research Reserve (MANERR) near Rockport, Texas, USA. Mangroves are established in the southern part of the

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MANERR, but, not in the north. Our study marshes were intertidal, experiencing similar tidal

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fluctuations (~ 0.5 meters) that are influenced by diurnal and semi-diurnal tides but primarily by

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prevailing southeast winds. Faunal samples were collected during periods of high monthly tides

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in June of 2013 (10 – 11 and 24 – 25) when the highest marsh and mangrove elevations were

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submerged. Water temperature was 29o C + 0.9o C and 30o C + 1.2o, and salinity was 32 + 2.3

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ppt and 34 + 1.8 ppt in sites with and without mangroves respectively.

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Vegetation Survey

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We measured relative tidal elevations of Spartina and black mangroves. Spartina will

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not grow in subtidal areas. Therefore, we used the boundary between Spartina and benthic

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habitats (mud flats or seagrass beds in this area) as our lowest elevation point (i.e. point zero).

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Then, using a laser level we calculated the tidal elevations in which Spartina and mangroves

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were found relative to point zero along a transect from the lowest tidal elevation landward. In

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marshes where black mangroves were established and abundant, mangroves were present at

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higher elevations above mean lower low water while Spartina was present only in a narrow

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band ~1-4 m wide at the lowest tidal elevations (closest to mean lower low water). In contrast,

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Spartina dominated at both low and high tidal elevations in areas without abundant mangroves

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(Figure 1, see results). Spartina elevations are reported from sites without mangroves because

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Spartina elevations are compressed in mangrove sites.

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Faunal Collections

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We classified marshes into two types: those with abundant black mangroves and those

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where black mangroves were rare. Black mangroves were found in higher tidal elevations, and

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to account for both mangrove presence and tidal elevation in our sampling, our collections

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were made in a 2x2 factorial design, with mangrove presence and tidal elevation as factors.

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Samples at each elevation were paired and were ~ 2-3 m apart. We collected community

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samples at 2 tidal elevations (~0.1 m and ~0.4 m above mean lower low water) in 15 sites with

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and 14 sites without mangroves (58 samples total). Our intent was collect 15 paired samples in

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each marsh type, but our sampler malfunctioned at the last site, leaving us with 14 paired

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samples in marshes without mangroves. We used the lowest tidal elevation that Spartina was

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present as an estimate of mean lower low water because Spartina will not grow subtidal.

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Sampling sites were separated by more than 150 m to cover a large spatial area. In marshes

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with established mangroves, samples in lower elevations were collected within Spartina and

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higher elevations samples were always collected within mangrove pneumatophores. In marshes

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without mangroves, samples at both low and high tidal elevations were collected within

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Spartina (Figure 1). Water depth was recorded at each sampling location, but, did not

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significantly influence community assemblages and is not reported. All faunal samples were

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collected during highest seasonal tides to ensure the highest tidal elevations were submerged.

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Figure 1 Marshes with black mangroves (top) and without black mangroves (bottom). Black mangroves were present only at higher tidal elevations in a near monoculture once established. Spartina dominated at low and high elevations when mangroves were not present. Nekton and infaunal samples were collected from both tidal heights in both types of marshes, and the tidal elevation of Spartina and black mangroves was measured. In this figure, higher tidal elevations are on the left and the arrows represent paired sampling locations in each marsh type.

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Nekton Communities Nekton were collected using a suction sampler, which has been successfully used in previous coastal wetland studies (Heck et al., 1995). A 0.25 m2 cylindrical plastic barrel (open at

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both ends) was placed over a selected salt marsh or black mangrove habitat and was firmly

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pressed into the substrate to prevent organisms from escaping. The barrel encapsulated either

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Spartina shoots or black mangrove pneumatophores, allowing us to collect organisms directly

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within that particular vegetation type. After the barrel was placed, water was suctioned for

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three minutes to ensure all organisms trapped within the barrel were collected. Preliminary

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sampling indicated that 3 minutes was sufficient time for collecting all organisms. Samples were

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placed into 250 µm mesh bags, labeled, and placed on ice. Upon returning from the field,

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samples were placed into buckets containing 10% formalin for one week, and then transferred

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to jars containing 45% isopropyl alcohol. All organisms were identified to the lowest taxonomic

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level possible for use in multivariate analyses. Total abundance of fish, shrimp, and crabs was

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calculated. Dry weight biomass was determined for all fish, shrimp, and crabs collected by

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drying samples at 90o C for 72 hours, and weighing them on an analytical balance to the nearest

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0.001 g. All individual fish were weighed together for each sample, as were shrimp and crabs, to

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create a single measure of biomass for that group.

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Infaunal Communities

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Infaunal organisms were collected using PVC cores. Two sediment cores (10 cm

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diameter x 10 cm depth) were taken at both low and high tidal elevations (4 total cores) in 5

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sites with and 5 sites without mangroves. The number of organisms in cores taken at the same

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tidal elevation were combined for analysis. Benthic cores were placed into 250 µm mesh bags, 9

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gently rinsed with seawater in the field to remove excess sediment, labeled, and placed on ice.

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Upon returning from the field, samples were placed into buckets containing 10% formalin for a

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period of one week, and then washed using a 500 µm sieve and transferred to jars containing

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45% isopropyl alcohol. Infaunal organisms were sorted from detritus and plant material using a

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dissecting microscope. Polychaetes were identified to family and all other organisms were

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identified to the lowest taxonomic level possible for use in multivariate analyses.

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Data Analysis

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Nekton and infaunal samples were examined separately using univariate analyses in

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JMP Pro 12 and multivariate analyses in PRIMER ™. For nekton, the total abundance of fish,

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crabs, and grass shrimp (Palaemonetes spp.), as well as the biomass of each group were

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compared using a two-way ANOVA with mangrove presence (present/absent) and tidal

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elevation (low/high) as fixed factors. For infauna, total abundance of the two most abundant

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groups: polychaetes and crustaceans were similarly analyzed using a two-way ANOVA with

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mangrove presence (present/absent) and tidal elevation (low/high) as fixed factors. Data were

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log transformed to meet assumptions of equal variances. For both nekton and infauna, we

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created metric, 2D MDS plots from mean values of communities in each sample. We also

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performed multivariate analyses on nekton and infaunal community assemblages within each

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sample using Analysis of Similarity (ANOSIM) in PRIMER ™ with mangrove presence as the

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factor. SIMPER analysis was also performed to determine which organisms contributed to

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dissimilarities between mangrove and Spartina habitats.

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Results

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Vegetation Survey Spartina was present at lower tidal elevations than black mangroves (median 0.35 m vs.

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0.44 m), although mangroves were found over a larger range of tidal elevations (Figure 2). In

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marshes sites without mangroves, Spartina was found in monocultures at both low and high

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elevations. In contrast, when black mangroves were abundant, Spartina was relegated to tidal

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elevations below ~0.2 m, and found in a narrow band bordering the dwarf mangrove forest

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(Figure 1). Areas with equal mixtures of mangroves and Spartina at the same tidal elevations

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were difficult to find and were not sampled.

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1.25

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0.5 0.25

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Figure 2 Box and whiskers plot for tidal elevations of Spartina alterniflora and black mangroves. Boxes show median with 25% and 75% quartiles, and whiskers are range of heights that each type of vegetation was found. Spartina heights are reported only for sites without mangroves because mangroves displace Spartina at its highest tidal elevations.

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meters

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Nekton Communities Grass shrimp were significantly more abundant and had more biomass in marsh sites without mangroves (p < 0.01, Figure 3, Tables 1, 2), but fish were significantly more abundant

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and more fish biomass was found in marsh sites that had abundant mangroves (p < 0.01, Figure

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3, Table 1, 2). Crab abundance and biomass did not differ significantly between marshes with

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and without mangroves (p = 0.38, p = 0.35, Figure 3, Table 1, 2). Tidal elevation was not a

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significant factor for any of the comparisons of grass shrimp, crab, and fish abundance or

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biomass for these organisms among sites (Figure 3, Table 1, 2). The interaction between tidal

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elevation and mangrove presence was not significant for crab and fish abundance nor for

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biomass of any of these groups, but the interaction term was significant (P=0.55) for grass

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shrimp abundance (Table 1, 2).

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A metric MDS plot revealed that the greatest differences among samples were from

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marshes with and without mangroves and not from low and high tidal elevations, which was

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consistent with univariate analysis on abundances and biomass of grass shrimp, crabs, and fish.

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Because tidal elevation did not have a significant effect and had a smaller effect on the

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community than mangrove presence, ANOSIM was performed using mangrove presence as a

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factor influencing community differences. ANOSIM revealed significant effects of mangrove

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presence on overall community assemblages (R = 0.101, p = 0.001). However, R values

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approaching 0, such as the 0.101 value found here, suggests high variability within the data set.

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Since nekton are highly mobile and capable of moving among areas, this variability is not

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unexpected. The greatest dissimilarity between communities was attributed to grass shrimp,

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brown shrimp (Penaeus aztecus), and blue crabs that were more abundant in areas without

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mangroves and mud crabs (Panopeidae, Xanthidae) that were more abundant in mangrove

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areas (Table 3).

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Table 1. ANOVA Results for abundances of shrimp, crabs, and fish. Grass Shrimp Abundance (F=4.033,52, P = 0.01) df

2.47

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0.002

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1.15

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P

8.34

0.006

0.01

0.93

3.88

0.055

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Sum of Squares

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Crab Abundance (F=4.033,43, P = 0.32)

Mangrove Presence Tidal Elevation Mangrove Presence*Tidal Elevation

Sum of Squares

df

F

P

0.99

1

0.77

0.38

2.78

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2.15

0.15

1.68

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1.30

0.26

df

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4.79

1

9.25

0.005

0.08

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0.15

0.70

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Fish Abundance (F=4.033,33, P = 0.04)

Source

Sum of Squares

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Table 2 ANOVA Results for biomass of shrimp, crabs, and fish. Grass Shrimp Biomass (F=5.233,52, P < 0.001) df

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>0.001

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>0.001

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F

P

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<0.001

0.02

0.89

0.001

0.99

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Sum of Squares

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Crab Biomass (F=1.173,43, P = 0.33)

Mangrove Presence Tidal Elevation Mangrove Presence*Tidal Elevation

Sum of Squares

df

F

P

0.32

1

0.89

0.35

0.87

1

2.4

0.12

0.24

1

0.66

0.41

df

F

P

1.99

1

8.77

0.006

0.003

1

0.01

0.90

0.15

1

0.66

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Fish Biomass (F=3.173,33, P = 0.04)

Source

Sum of Squares

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Grass Shrimp Abundance 50 40

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Mean Abundance

Crab Abundance

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High

Fish Abundance

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Spartina

Low 270

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High

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Figure 3 Mean + SE abundances of shrimp, crabs, and fish in samples from high and low tidal elevations from marshes with and without mangroves. Shaded bars are high tidal elevations, and x axis labels are marshes with abundant mangroves vs. those with only Spartina. Significant differences were found for shrimp and fish at α = 0.05. Significant differences between tidal elevations were not found.

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Metric MDS

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Resemblance: S17 Bray-Curtis similarity 2D Stress: 0.01

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MG + Low Yes/Low MG + High Yes/High No/Low MG - Low No/High MG - High

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MDS2

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0 MDS1

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2D Stress: 0.25

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MDS2

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Metric MDS

Transform: Square root Resemblance: S17 Bray-Curtis similarity

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0 MDS1

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Figure 4 Metric MDS plot showing (A) mean and (B) all distances between nekton samples from marshes with and without mangroves at low and high tidal elevations. Black triangles indicate mangroves were present (MG+), and white triangles indicate they were absent (MG-). Triangles point up for high elevation and down for low elevation.

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Table 3 SIMPER analysis for nekton. Abundances shown were square root transformed for analysis.

Grass shrimp (Palaemonetes) Mud crabs (Xanthidae/ Panopeidae) Brown shrimp (Penaeus aztecus) Blue crabs (Callinectes sapidus)

Mangrove Mean Abundance 2.71

Spartina Mean Abundance 4.74

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1.59

1.05

9.9

0.58

0.91

5.9

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0.48

3.6

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Mangrove vs. Spartina Dissimilarity % Contributed

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29.8

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Species

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Infaunal Communities Polychaetes were significantly more abundant in marsh sites without mangroves (F1, 1 = 4.43, p = 0.06), while tidal elevation did not significantly affect polychaete abundance (F1, 1 =

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0.67, p = 0.43), and the interaction between mangrove presence and tidal height was not

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significant (F1, 1 = 0.55, p = 0. 47). Over 95% of the crustaceans collected were from the

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Tanaididae family. Like polychaetes, crustaceans, were significantly more abundant in marsh

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sites without mangroves (F1, 1 = 7.24, p = 0.03). Tidal elevation did not significantly affect

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crustacean abundance (F1, 1 = 0.14, p = 0.71), and the interaction between mangrove presence

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and tidal height was not significant (F1, 1 = 0.01, p = 0.97). Similar to nekton findings and

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consistent with ANOVA results, a metric MDS plot revealed that the greatest differences among

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infaunal communities were from samples taken from marshes with and without mangroves and

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not between tidal elevations (Figure 6). ANOSIM revealed significant effects of mangrove

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presence on infaunal community assemblages (R = 0.62, p = 0.001). The global R value for

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mangrove effects on infaunal communities was much higher than found for nekton

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communities, probably because infaunal communities are far less mobile than nekton. The

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greatest dissimilarity between communities was attributed to Tanaidae, Nereididae,

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Amphipods, and Capitellidae (Table 4).

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Polychaetes

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25 325

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20 15

5 0

Crustaceans 40 30 20

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Mangrove

Low

339 340 341

328 329 330 331 332

Spartina

High

333

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Figure 5. Mean + SE abundances of polychaetes and crustaceans from infaunal samples collected in high and low tidal elevations from marshes with and without mangroves. Shaded bars are high tidal elevations, and x axis labels are marshes with abundant mangroves vs. those with only Spartina. Significantly more polychaetes and crustaceans were found in marshes without mangroves at α = 0.05. Significant differences between tidal elevations were not found.

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Mean Abundance

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10

342 343

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Metric MDS Resemblance: S17 Bray-Curtis similarity

345

2D Stress: 0.06

XXXXXXXXXXX Yes-Low XXXXXXXXX

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XXXXXXXXXXX No-Low XXXXXXXXX

Yes-Low MG + Low MG + High Yes-High MG - Low No-Low MG - High No-High

MDS2

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350 351

XXXXXXXXXXX No-High XXXXXXXXX

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0 MDS1

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365 366 367 368

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Metric MDS

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50

356

364

20

Transform: Square root Resemblance: S17 Bray-Curtis similarity

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363

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0 MDS1

359 360

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100

Figure 6 Metric MDS plot showing (A) mean and (B) all distances between infaunal samples from marshes with and without mangroves at low and high tidal elevations. Black triangles indicate mangroves were present (MG+), and white triangles indicate they were absent (MG-). Triangles point up for high elevation and down for low elevation.

369 370 371 23

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372 373 374

Table 4 SIMPER analysis for infauna. Abundances shown were square root transformed for analysis.

Tanaidae Nereididae Amphipod Capitellidae

Spartina Mean Abundance 2.69 1.28 1.51 1.04

23.4 14.5 13.2 10.2

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Mangrove vs. Spartina Dissimilarity % Contributed

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Species

Mangrove Mean Abundance 0.14 1.23 0.34 0

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24

27.9 17.3 15.8 12.2

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Discussion Climate change and invasion of exotic species, which in some cases are facilitated by a warming climate, are altering foundation species in coastal wetlands ( Gonzalez et al.; 2010,

381

Barbier et al., 2011; Comeaux et al., 2012), often with profound impacts on ecosystem

382

processes and associated fauna (Micheli et al. 2008; Armitage et al. 2015). Invasion by the

383

common reed (Phragmites australis) decreased faunal abundance and diversity in US Atlantic

384

salt marshes ( Osgood et al., 2003; Kimball et al., 2010) as did changes in seagrass species in

385

North Carolina (Micheli et al., 2008) and Texas (Ray et al., 2014). Expansion of mangroves into

386

salt marshes has occurred in North and South America and Australia, decreasing marsh habitat

387

(Saintilan et al., 2014). In the Gulf of Mexico, black mangroves are displacing Spartina and other

388

marsh plants (Armitage et al., 2015), altering wetland elevations and ecosystem processes such

389

as nutrient cycling (Comeaux et al., 2012).

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Our findings indicate that changes from Spartina dominated to mangrove dominated coastal wetlands will have significant impacts on associated fauna in the Gulf of Mexico.

392

Infaunal communities, blue crabs, and both grass and brown shrimp were less abundant in

393

marshes with abundant mangroves, even when collected from low tidal elevations where

394

Spartina was present. In contrast, mud crabs and fish were more abundant in marshes

395

dominated by mangroves. Similarly, Lunt et al. (2013) found infauna to be lower in mangrove

396

areas. In Louisiana, mangrove effects on nekton differed from those report here (Caudill 2005),

397

with fish more abundant in marsh sites and shrimp more abundant in mangrove areas. Caudill’s

398

differing findings may be related to methodology as they used lift nets to capture organisms on

399

outgoing tides and their community composition was differed considerably. We found few gulf

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killifish Fundulus grandis and no white shrimp Litopenaeus setiferus, but, both were abundant

401

in Caudill’s 2005 study. Further, grass shrimp were abundant in our study but and rarely

402

collected by Caudill (2005), perhaps due to variation in sampling gear. Regardless of whether

403

differences in these studies result from different sampling methods or different communities in

404

the northern vs. southern Gulf of Mexico, both studies suggest mangroves affect faunal

405

composition. Our findings indicate mangrove presence influenced associated marsh fauna in

406

adjacent areas that were dominated by other plant species (i.e. Spartina). We do not yet know

407

how mangroves are influencing wetland species but hypothesize that mangroves alter food

408

webs through changes in the outcomes of predatory interactions (Hammerschlag et al., 2010)

409

and/or by affecting abiotic conditions and resource availability to make habitats less suitable for

410

some species (Alongi et al., 2004; Castañeda-Moya et al., 2013; Comeaux et al., 2012).

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Black mangrove edge habitats are used by predators as hunting corridors

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(Hammerschlag et al., 2010), and mangrove encroachment into Spartina marshes may alter

413

food webs by changing the foraging environment for predators and prey. In sites with

414

mangroves, fish and crabs were more abundant while infaunal organisms and grass shrimp,

415

common prey items for fish and crabs, (Kneib and Wagner, 1994), were less abundant.

416

Mangroves accumulate sediment, raising the tidal elevation and reducing emergence time for

417

the areas where they are found (Comeaux et al., 2012). Thus, common wetland aquatic species

418

would spend less time in the highest tidal elevations and more time in the fringing Spartina

419

marshes. By altering the landscape, mangroves may place predators and prey in close proximity

420

and concentrate them by reducing suitable habitat area, thereby altering encounter rates,

421

predation levels, and food web structure.

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422

Additionally, resource availability via detrital inputs is vastly different from woody mangroves and Spartina, and likely influence food webs through bottom-up forces (Alongi,

424

1998; Alongi et al., 2004; Castañeda-Moya et al., 2013). Geochemical processes, sediment

425

accretion, and carbon sequestration and turnover differ significantly among black mangrove

426

and Spartina habitats (Alongi et al., 2004; Castañeda-Moya et al., 2013; Comeaux et al., 2012),

427

and the distribution of organisms, particularly infaunal species, are often influences by changes

428

in these factors (Baguley et al., 2006). Mangroves may simultaneously influence both top-down

429

and bottom-up factors, thereby influencing the diversity and abundance of associated fauna.

430

Clearly more research is needed to elucidate the mechanisms by which mangroves affect

431

associated fauna.

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432

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Tidal elevation and inundation often have significant effects on coastal communities, influencing nekton abundance in coastal wetlands ( Rozas and Minello 1998; Rozas and

434

Zimmerman 2000). Brown shrimp and grass shrimp can be more abundant at lower tidal

435

elevations (Minello et al., 1994), but in our study, tidal elevation did not significantly affect

436

community assemblages or abundances of individual organisms. Consistent with our findings,

437

communities in Chesapeake Bay were not significantly different in salt marshes between low

438

and high tidal elevations (Posey et al., 2003). We sampled at the lowest tidal elevations possible

439

that would allow us to collect organisms in both Spartina and mangrove areas, and perhaps the

440

differences in tidal elevations were not large enough to observe differences seen in other

441

studies (Rozas and Zimmerman 2000). Regardless, the presence of mangroves influenced

442

community composition at the lowest elevations that were dominated by Spartina,

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443

independent of tidal height sampled, which provides strong evidence that mangroves are

444

influencing wetland fauna. Vegetation shifts are occurring across the globe in response to anthropogenic effects

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including climate change (Gonzalez et al., 2010), which can alter fauna that utilize these

447

habitats (Micheli et al., 2008; Ray et al., 2014). Both nekton and infaunal communities were

448

significantly different in locations where mangroves became established, suggesting that

449

mangrove expansion into marsh areas previously dominated by Spartina will have significant

450

effects on estuarine food webs and biodiversity. Our results provide a baseline for future

451

studies examining effects of mangrove encroachment on fauna that inhabit coastal wetlands.

452

The mechanisms by which mangroves are affecting fauna and the broader ecosystem

453

consequences of faunal changes requires further investigation, but understanding how these

454

changes affect alter species diversity and abundance are necessary for management,

455

mitigation, and conservation of coastal wetlands and associated species.

456

Acknowledgements

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Funding was provided by the US Forest Service Southern Research Station agreements 12-DG-11330101-096 and 13-CA-11330140-116 to D.L. Smee. The NSF-MSP ETEAMS grant

459

#1321319 provided funding for boat time and their interns assisted in the field. Members of the

460

Marine Ecology Lab including J. Lunt and A. Scherer, and Julie Arnold and Christina Stringer

461

from USFS provided important assistance in the field for both collections and measurements of

462

vegetation tidal elevations. Students in TAMU-CC’s REU program also provided field help. S.

463

Bock was instrumental for writing and data analysis.

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2 0 1 0 0 0 0 0 0 0 0 0 0 0 7 1 7 0 4 0 0 0 7 0 3 0 4 0 0 0 10 1 6 0 16 1 9 3 1 0 0 0 14 0 0 0 1 0 5 0 27 7 21 5 13 12 24 65

0 0 1 0 0 0 0 0 0 0 2 0 1 2 1 0 0 0 0 0 0 0 0 1 1 0 0 0 1 1 1 3 1 0 0 1 0 3 1 0 0 0 0 0 0 2 0 0 0 0 0 1 1 0 0 3 4 0

Atlantic Thinstripe Dark Shore Crab Hermit Crab Mud Crab

Eurypanopeus turgidus

Panopeus herbstii

Pachygrapsus gracilis

0 0 0 0 0 0 1 0 0 0 2 0 1 0 2 0 0 0 2 0 0 0 1 0 0 0 0 0 3 1 2 0 0 0 0 1 0 1 0 0 0 2 1 1 0 0 0 0 0 0 4 1 0 0 3 1 0 1

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 6 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 3 1 0 1 0 0 2 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 13 0 3 1 0 0 1

Diamond Killifish

Clibanarius Adinia vittatus xenica 0 3 0 0 1 0 0 1 0 0 0 0 0 1 2 2 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 1 0 0 0 0 2 0 2 2 2 4 2 1

0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 1 3 0 1 1 0 0 0 0

Sheepshead Minnow

Pin Fish

Striped Mullet

Darter Goby

Naked Goby

Gobies (Unknown)

Longnose Mosquito Sailfin Molly Killifish Fish

Cyprinodon variegatus

Lagodon rhomboides

Mugil cephalus

Ctenogobius boleosoma

Gobiidae

Gobiidae

Funduls similis

Poecilia latipinna

0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 6 1 1 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 7 1 1 0 1 1 0 5 0 0

3 0 0 0 0 0 0 0 0 0 1 0 1 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

3 0 0 0 0 0 1 0 0 7 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 0 0 0 0 0 0 0

0 0 0 0 0 0 0 1 1 0 1 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 0 7 0 0 1 0 1 0 0

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 0 1 0 1 0 1 1 0 0 1 2 0 1 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 0 0 1 0 1 1 0 1 0 0 0 0

0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0

Gulf Toadfish

Gulf Pipefish

Inland Silverside

Mangroves Present

Tidal Elevation

Depth

Gambusia affinis

Opsanus beta

Syngathus scovelli

Menidia beryllina

Yes or No

Low or Higy

cm

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 1 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0

Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes No No No No No No No No No No No No No No No No No No No No No No No No No No No No Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes

Low High Low High Low High Low High Low High Low High Low High Low High Low High Low High Low High Low High Low High Low High Low High Low High Low High Low High Low High Low High Low High Low High Low High Low High Low High Low High Low High Low High Low High

37 19 35 21 30 15 35 19 19 13 35 17 23 11 26 20 24 19 30 14 19 8 42 20 30 24 32 22 30 20 30 24 31 20 32 17 22 16 34 22 29 13 45 14 27 21 29 21 17 9 23 8 33 13 36 19 19 24

RI PT

Panopeidae Callinectes Xanthidae sapidus

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 3 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

Ridgeback Mud Crab

SC

Alpheidae

Blue Crab

M AN U

Mud Crabs

TE D

Penaeus Palaemonetes aztecus 4 1 14 5 4 2 4 2 8 2 6 0 12 2 7 0 6 0 0 0 18 2 15 0 9 2 31 0 2 0 28 1 35 0 4 0 29 0 18 0 1 0 1 0 13 0 2 0 31 2 24 1 22 4 29 5 15 3 75 9 46 1 3 1 41 10 4 1 119 0 95 0 71 1 106 3 19 1 16 0 0 0 9 0 54 0 21 1 0 1 47 2 0 0 2 0 1 0 0 0 1 0 9 0 1 0 16 0 1 0 2 2 3 2 7 3

Snapping Shrimp

EP

Brown Shrimp

AC C

Grass Shrimp

ACCEPTED MANUSCRIPT

isopod 0 0 0 0 0 0 0 0 0 0 0 0 3 0 6 3 0 0 1 0

Copepod 0 0 0 0 5 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

Palaemonetes 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0

RI PT

Amphipod 0 1 0 0 0 2 0 0 0 0 2 1 14 1 3 3 0 3 1 3

SC

Tanaidae 1 0 0 0 0 0 0 0 0 0 25 6 54 17 0 2 5 3 0 7

M AN U

Spionidae 0 0 0 0 0 0 0 0 0 0 2 1 1 0 0 0 0 0 1 0

TE D

Oligochaete 0 0 0 0 0 0 0 0 0 0 0 36 2 2 0 0 0 0 0 1

EP

Capitellidae 0 0 0 0 0 0 0 0 0 0 0 17 0 0 0 3 2 0 10 0

AC C

Nereididae 2 3 6 1 0 1 0 0 0 1 14 2 9 7 0 4 0 0 0 0

Mangroves Present Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes No No No No No No No No No No

Low or High Elevation Low High Low High Low High Low High Low High Low High Low High Low High Low High Low High

Depth 37 cm 19 cm 35 cm 21 cm 30 cm 15 cm 35 cm 19 cm 19 cm 13 cm 19 cm 8 cm 30 cm 12 cm 42 cm 20 cm 30 cm 24 cm 32 cm 22 cm