Hydrobiologia 436: 17–33, 2000. © 2000 Kluwer Academic Publishers. Printed in the Netherlands.
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Biogeography of benthic macroinvertebrates in estuaries along the Gulf of Mexico and western Atlantic coasts1,2 Virginia D. Engle∗ & J. Kevin Summers U.S. Environmental Protection Agency, National Health and Environmental Effects Research Laboratory, Gulf Ecology Division, 1 Sabine Island Drive, Gulf Breeze, FL 32561, U.S.A. E-mail:
[email protected] ∗ Author for correspondence Received 7 July 1999; accepted 20 June 2000
Key words: biogeography, estuary, benthic, invertebrate, province
Abstract The community composition of benthic macroinvertebrates from 870 estuarine sites was examined in order to either confirm or challenge established boundaries of biogeographical provinces along the Gulf of Mexico and western Atlantic coasts of the United States. The objective was two-fold: (1) to demarcate boundaries that separate dissimilar fauna in the Gulf of Mexico, and (2) to compare the Gulf of Mexico biogeographically with other wellknown provinces. We segmented the coastline into grid cells with dimensions of 1◦ latitude and 2–4◦ longitude. Using the descriptive techniques of cluster analysis and nonmetric multidimensional scaling, we determined the similarities in benthic community composition between sites within grid cells in the Gulf of Mexico and compared the biotic ordinations to natural habitat characteristics such as salinity, sediment type, and depth. We then evaluated the overall community composition within each grid cell in the Gulf of Mexico and established whether or not similarities existed between adjacent grid cells. In this manner, we confirmed that an east–west gradient existed in estuarine benthic community composition along the Gulf of Mexico coast. This information was combined with our previous work in the western Atlantic coast to discern biogeographical provinces. Based on cluster analyses and an analysis of endemic benthic species the following provinces are proposed: (1) the Virginian province, from Cape Cod, Massachusetts to Wilmington, North Carolina, (2) the Gulf of Mexico, from Rio Grande, Texas to Cape Romano, Florida, and (3) south Florida, south of latitude 26◦ N. The region encompassing South Carolina, Georgia and northern Florida represents a transitional area between temperate and tropical provinces.
Introduction Biogeographers have historically associated the latitudinal distribution of marine fauna with temperature or oceanic currents (Hutchins, 1947; Ekman, 1953, Hall, 1964; Cerame-Vivas & Gray, 1966; Valentine 1966; Briggs, 1974; Cox & Moore, 1993). Along the Atlantic and Gulf of Mexico coasts of the United States, five provinces have been delineated according 1 Contribution No. 1067 of the U.S. Environmental Protection Agency, National Health and Environmental Effects Laboratory, Gulf Ecology Division, Gulf Breeze, Florida 32561. 2 The mention of commercial products or trademarks does not constitute endorsement or recommendation by the U.S. Environmental Protection Agency.
to climate and oceanic currents: Acadian, Virginian, Carolinian, West Indian and Louisianian provinces (see Figure 1; Hutchins, 1947; Ekman, 1953; Hall, 1964; Gosner, 1971; Briggs, 1974). The coincidence of marine biogeographical and climatic provinces and the location of provincial boundaries have been debated by biogeographers since Forbes’ (1856, as cited in Briggs, 1974) maps of the distribution of marine life. Biogeography encompasses the analysis and explanation of observed patterns in the distribution of organisms (Hedgpeth, 1957; Hall, 1964; Golikov et al., 1990; Cox & Moore, 1993). The first task in biogeography is to examine the similarities and differences among fauna from large regions and to define
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Figure 1. Map of the western Atlantic and Gulf of Mexico coasts with provinces as delineated by EMAP-E and landmarks as discussed in the text.
provinces by drawing boundaries between dissimilar distributions of organisms (Myers & Giller, 1988; Hengeveld, 1990). Often provincial boundaries have been defined by a combination of endemism, similarities among geographical assemblages of species, and geological or geographical features that provide convenient points of demarcation (Rosen, 1988). Delineating boundaries between provinces implies that a barrier exists that prevents biotic exchange (Brown & Gibson, 1983). Marine provinces, therefore, have been most sharply defined along continental coast lines where geographical landmarks (capes or points) mark not only a convergence or divergence of oceanic currents but also a distinct change in marine fauna (Coomans, 1962; Cerame-Vivas & Gray, 1966; Brown
& Gibson, 1983). The biogeographical provinces for marine fauna of the western Atlantic have been wellestablished, while the faunal distributions in the Gulf of Mexico have been comparatively less well-studied (Johnson, 1934; Briggs, 1974). Although Hedgpeth (1953) reviews the early pre-1950 knowledge of the zoogeography of the Gulf of Mexico, he cautions (1953; p. 205) that, because quantitative bottom community investigations had yet to be made in Gulf of Mexico and western Atlantic waters, a comprehensive synthesis of biogeographical information was not available. The majority of modern biogeographers agree, however, that the northern Gulf of Mexico fauna inhabit a warm-temperate region and that the boundaries between temperate and tropical provinces
19 in the Gulf occur on both the Texas and Florida coasts roughly between latitude 26◦ and 30◦ N (see review by Briggs, 1974). Some researchers refer to a high degree of endemism in the northern Gulf of Mexico, indicating that this region should be recognized as a unique province, while others include the northern Gulf of Mexico as part of either the warm-temperate Carolinian province or the tropical West Indian province (Stephenson & Stephenson, 1952; Hedgpeth, 1953; Rehder, 1954; Moore, 1961; Cerame-Vivas & Gray, 1966; see review by Briggs, 1974). Much of the biogeographical work that has been done previously has been limited to a single faunal group (e.g. bivalves, molluscs, tunicates or fish) or to marine organisms that inhabit the shallow near-shore environment exclusively. Stephenson & Stephenson (1950) recognized the need to examine the distributions of a fauna as a whole community and they used intertidal biota to suggest biogeographical divisions along the North American coast. Establishing biogeographical provinces based on estuarine fauna has been problematic due to the complex, natural gradients (i.e. salinity, sediment type or depth) that define local community composition in estuaries. Engle & Summers (1999a), however, successfully delineated provinces along the western Atlantic coast using estuarine benthic macroinvertebrates. The current paper is the second in a series of biogeographical analyses that builds on our previous work by extending the analysis into estuaries in the Gulf of Mexico. Our primary purpose was to examine the distribution of benthic macroinvertebrates from estuaries in the Gulf of Mexico in order to determine if, indeed, two provinces were represented in this region and, if so, determine the location of the boundary between temperate and tropical fauna. Our secondary objective was to determine if the Gulf of Mexico should be considered a unique biogeographical province or if the fauna had enough similarities to the fauna of the western Atlantic that the Gulf of Mexico should be considered to be an extension of an Atlantic province. We analyzed benthic macroinvertebrate community composition data that were collected within the framework of the U.S. Environmental Protection Agency’s (U.S. EPA) Environmental Monitoring and Assessment Program for Estuaries (EMAP-E). This analysis accomplished one of the objectives of EMAP-E, which was to determine the geographical distribution of ecological resources within and among biogeographical provinces (Summers et al., 1995). Although EMAP-E was neither designed nor intended
specifically for biogeography, both the sample design and the data collected were conducive to answering traditional biogeographical questions. Early biogeographical studies relied on gathering species lists or information on range limits and distributions from published papers because large, standardized data sets were not available (e.g. Coomans, 1962; Valentine, 1966; Hayden & Dolan, 1976; Calder, 1992). Our study benefits from data that was collected across a large geographical area within the confines of a national environmental monitoring program that relied on standardized protocols for all aspects of sample collection and analysis. We defined grid cells similar to those used by Hayden & Dolan (1976) to partition the coastline into spatial units of approximately equal size. We examined the similarities of benthic communities within grid cells defined by latitude and longitude and compared the observed similarities to habitat characteristics (i.e. salinity, depth and sediment type). We then investigated the similarities between benthic communities in adjacent grid cells using cluster analysis and nonmetric multidimensional scaling. Cluster analysis is a useful tool that enables biogeographers to identify areas with similar community composition in a quantitative manner (Valentine, 1966; Calder, 1992; Kendall & Aschan, 1993; Diaz, 1995; Mahon et al., 1998). We determined breakpoints along the Gulf of Mexico coast as defined by differences in benthic macroinvertebrate community composition in estuaries. Extending the grid up the Atlantic coast to latitude 41◦ N, we used cluster analysis and an analysis of endemism to make a final determination on the nature of western Atlantic and Gulf of Mexico biogeographical provinces. We compared our findings with established provincial boundaries and speculated on how this type of analysis could aid investigations of potential impact of anthropogenic stressors associated with recent global climate change scenarios on the distribution of benthic macroinvertebrates.
Methods Phase I: Gulf of Mexico EMAP-E collected benthic samples in Gulf of Mexico estuaries from Florida Bay, Florida, to the TexasMexico border during a five year period (Figure 1). Based on established biogeographical boundaries, EMAP-E divided the Gulf of Mexico coast into two
20 provinces (Louisianian and West Indian) and this study incorporated data from both of these provinces. EMAP-E employed a probabilistic design to select 507 sampling stations within a triangular grid framework. Stations were located in the subtidal zone of estuarine systems along the Gulf of Mexico coast. Both provinces adhered to all aspects of the EMAP-E sampling design from the probabilistic station matrix to the collection and quality control of benthic invertebrate samples (Summers et al., 1991). EMAPE chose to sample during a summer index period to represent the time frame during which the most severe impacts of natural and anthropogenic stressors on the biota would be expected to occur (Summers et al., 1995). Each station was sampled once during the summer months of 1991–1994 in the Louisianian province and of 1995 in the West Indian province. No station was sampled more than once during the same year and a different, probabilistic selection of stations was sampled each year. Standardized methods were employed for collecting samples in the field and processing samples in the laboratory, thus ensuring standardization of procedures for the entire data set. At each site, at least three replicate benthic samples were collected using a Young-modified Van Veen grab that sampled a surface area of 440 cm2 . Because stations were located in the subtidal zone of estuaries, primarily soft-bottom habitats were sampled. Samples were sieved in the field and the fauna, retained on a 0.5 mm screen, were preserved in rose-bengal buffered formalin. At the laboratory, samples were sieved again on a 0.5 mm screen, sorted into major taxonomic groups and then individuals were identified to lowest practical taxonomic level and counted. Due to difficulties encountered during sample processing at the laboratory, only one grab per station was evaluated for the West Indian province. Because all of the taxonomy was performed by the same laboratory, all taxonomic records, including those with laboratory-specific identifications (e.g. sp. A or sp. 1), were considered to be unique and were retained in the data set. The sampling gear was designed specifically to sample soft-bottom macroinvertebrate infauna. Any chordates (i.e. fish, cephalochordates [Amphioxus], urochordates [tunicates] and hemichordates [acorn worms]) or meiofauna (e.g. copepods, nematodes) that were identified by the laboratory were considered to be accidental inclusions and were omitted from the data set. To characterize water quality at each station, salinity, temperature, pH, and dissolved oxygen were recorded at 1 m intervals from the surface to the bot-
tom by a Hydrolab Surveyor II. Depth at the station was recorded from the boat’s fathometer. Sediment samples for grain size analysis were homogenized from the top 2 cm from several grabs and sent to separate laboratories for determination of silt-clay and sand fractions and for an analysis of a suite of organic and inorganic chemical constituents (see Summers et al., 1991). Because our interest was in benthic community composition based on natural gradients, it was desirable to omit all stations with degraded sediment quality that could be attributed to an anthropogenic origin. By so doing, we removed the potential for the benthic community composition at a station to be determined by confounding anthropogenic influences rather than natural habitat characteristics. Ecological indicators for determining whether or not a station had degraded sediment quality were developed by both EMAP-E provinces. For both provinces, we omitted all stations that had a low benthic index, and where at least one of the following conditions was true: 1. at least three contaminants had concentrations greater than ER-L guidelines or at least one contaminant was greater than ER-M guidelines (Long et al., 1995), 2. control-corrected survival of the amphipod, Ampelisca abdita (Mills, 1964), from sediment toxicity tests was less than 80%, or 3. bottom dissolved oxygen concentrations were less than 2 mg l−1 . The ER-L and ER-M guidelines delineate concentrations of contaminants at which adverse biological effects occur rarely (< ER-L), occasionally (between ER-L and ER-M), or frequently (> ER-M). They were developed by Long et al. (1995) from a biological effects database that contained the concentrations of contaminants at which adverse biological effects were measured (i.e. altered benthic communities, sediment toxicity and histopathological disorders in demersal fish). The benthic index for each province represented a combination of diversity and abundances of indicator taxa that was used to discriminate stations with degraded benthic communities. The components and threshold values, however, were slightly different for the Louisianian and West Indian provinces (Engle & Summers, 1999b; Macauley et al., 1999). These omissions reduced the number of stations that were used in the analyses to 410 (from a total of 507). In the first phase of the analysis, stations were grouped arbitrarily into numerically coded grid cells with a latitudinal thickness of 1◦ (Figure 2) similar to the method of Hayden & Dolan (1976). Because the Gulf of Mexico coast has a dominant east-west trend,
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Figure 2. Map of western Atlantic and Gulf of Mexico coasts with grid cells and latitude / longitude shown.
we added longitudinal divisions that ranged from 2◦ to 4◦ to provide a set of grid cells that covered the coast line with spatial units of approximately equal size. An arbitrary division of coastline into 1◦ latitudinal increments was also used by Valentine (1966) who noted that this subjective partitioning of the data resulted in variation in sample size, especially in the in-shore and shallow-water habitats. The same is true of our design where the number of stations in our grid cells ranged from four to ninety-one. Because of the variable size and location of estuaries, however, the variation in sample size introduced by the arbitrary selection of grid cells was unavoidable. Since all benthic taxonomy was completed at the same laboratory, we used data at the species level. All taxa that were listed as ‘unidentified’ at a taxo-
nomic level higher than species were omitted from this exercise. Transformation of abundance values using loge (1+x) enabled us to effectively evaluate patterns in the entire community by properly weighting both common and rare species (Clarke & Warwick, 1994). All statistical analyses were accomplished using SAS/STATr procedures (SAS Institute, 1990). Within a grid cell, a matrix was created consisting of all stations as rows and all genera as columns. The Bray-Curtis (dis)similarity coefficient, which does not count mutual absences (Clarke & Warwick, 1994), was calculated for every pair of stations. Classification of sites was accomplished by performing averagelinkage cluster analysis on the matrix of Bray-Curtis dissimilarities, resulting in a dendrogram that plotted clusters by distance. Station clusters were identified
22 by drawing a line on the dendrogram at distance=1.0. This subjective demarcation of clusters corresponded to a Bray-Curtis similarity of 10–30%. Multidimensional scaling (MDS) was performed on the (dis)similarity matrix. The station groups identified by cluster analysis were transferred to the MDS plot and then overlaid with labels representing the classification of salinity, sediment, or depth values, or with estuary names. For classification purposes, stations were grouped by bottom salinity into tidal freshwater (0–0.5%), oligohaline (0.5–5%), low mesohaline (5–12%), high mesohaline (12–18%), polyhaline (18– 35%) and marine (>35%). Similarly, stations were also classified by sediment type as sand (80% silt-clay). Overlaying classifications of salinity, sediment, or depth values can be used to visualize which environmental factors are best associated with the cluster of stations determined by the dissimilarity coefficients (McRae et al., 1998). The results from this phase of the analysis were used to identify patterns of similar benthic communities within each grid cell. The MDS plot suggested which combination of environmental factors, like salinity, sediment type, or depth, provided the ‘best’ match to the similarities among benthic communities. From this analysis, we determined which, if any, environmental factors were highly correlated with the benthic community composition. These factors would be taken into account during the analysis to detect biogeographical differences across the Gulf of Mexico. Next, the entire benthic community was grouped by grid cells and any important environmental factors, and similarities and dissimilarities among grid cells across the Gulf were identified using the same clustering and MDS techniques. In order to make these comparisons, the mean abundance of each taxa over all stations within each grid cell was calculated. Then a matrix of all grid cells as rows and all taxa as columns was created and all missing abundances were converted to zeros. The Bray-Curtis coefficient was calculated for all pairs of grid cells. Cluster analysis and MDS were applied as before and the results were plotted as dendrograms and MDS ordinations.
Phase II: Gulf of Mexico and Atlantic The second phase of analysis incorporated results from our previous work on establishing latitudinal gradients in benthic macroinvertebrate community
composition along the Atlantic coast of the U.S. (Engle & Summers, 1999a). We combined the data from the Gulf of Mexico estuaries with the data from Atlantic coast estuaries, which was also collected by EMAP-E using the same protocols. The benthic taxonomy was performed at several different laboratories which introduced a potential for redundancy or overlap of taxonomic nomenclature. To circumvent this problem, we omitted from the data set any unidentified genera or species, all records where the lowest taxonomic level was higher than species, all records with laboratory-specific identifications (e.g. sp. A or sp. 1), and all records of mixed species (e.g. when the species was recorded as ‘convexa & fornicata’). We extended the grid cell designations north along the Atlantic coast, from latitude 25◦ N to 41◦ N (see Figure 2), using the same numbering system as in Hayden & Dolan (1976). Each grid cell represented 1◦ latitude and, in the state of Florida, longitudinal boundaries were assigned so that there was no overlap within a grid cell of Gulf and Atlantic data. The final data set included benthic data from 31 grid cells (259–290, excluding grid cell, 275, where no data was collected) and represented benthic macroinvertebrate community composition in estuaries extending from the Rio Grande, Texas to Cape Cod, Massachusetts. The final data set contained 1100 benthic species from 870 undegraded stations sampled in 1990–1993 in the Virginian Province, 1994–1997 in the Carolinian Province, 1995 in the West Indian Province and 1991– 1994 in the Louisianian Province. The Bray-Curtis coefficient was calculated for all pairs of grid cells. Cluster analysis and MDS were applied as described earlier and the results were plotted as dendrograms and MDS ordinations. In order to validate the biogeographical clusters that resulted from cluster analyses, we also examined the degree of endemism within each cluster. We considered the major clusters to approximate provinces and conducted analyses in this context. A biogeographic province should have a high degree of endemism near the center of its range, while the edges or boundaries of the province should be populated with fewer endemic species and more transitional or ubiquitous species (Hedgpeth, 1953). Using the five clusters that were identified from this analysis, endemic benthic species were defined as occurring only within a single cluster. We then calculated the proportion of the benthic species within each grid unit that were endemic to the corresponding cluster.
23 Results Phase I: Gulf of Mexico A total of 956 taxa were identified from the EMAP-E Gulf of Mexico estuarine samples. At stations within each grid cell, the benthic communities clustered mainly along salinity gradients, either alone or in combination with sediment and, occasionally, depth gradients. Depth was rarely a determining factor as Gulf of Mexico estuaries are usually shallow ( 12%) are presented here. For the high salinity zone (>12%) the grid cells clustered in three groups from east to west (Figure 3). Grid cells, 272 and 273, clustered entirely separately from the rest of the region and included Florida Bay in the West Indian province. A second cluster also included stations in grid cells, 270 and 271, which covered Tampa and Sarasota Bays and Charlotte Harbor in the West Indian province. The grid cells, 259– 269 formed the third cluster, encompassing the entire Louisianian province. The cluster analysis for the low salinity zone (≤12%) produced similar groups. Several grid cells, however, were omitted from this analysis. There were no low salinity stations in grid cells, 259, 260, 267, 270 or 273. Regardless of the reduction in the number of grid cells, they clustered from east to west into three
groups: (1) grid cells, 269 and 272, (2) grid cell, 271, and (3) 261–268. Even though salinity was a major determining factor in the local distribution of benthic species and salinity zones were not evenly distributed along the Gulf of Mexico coast, the cluster analyses for different salinity groups produced very similar results (i.e. separating the Louisianian and West Indian provinces). Based on these results, we recombined the data and performed the cluster analyses on all data without regard to salinity. Again the grid cells clustered from east to west in three groups similar to those described previously for the high salinity zone (Figure 4). The following section details the results of this cluster analysis using all of the data. The southeastern-most cluster, represented by Florida Bay (grid cells, 272 and 273), was characterized by predominantly polyhaline, shallow (12 ppt) stations only.
Table 1. Top 10 benthic species that contribute to the dissimilarity between two adjacent clusters, Florida West Coast (grid cells, 267–271) and Florida Bay (grid cells, 272–273), listed by their average abundances and average dissimilarity Species
Polychaeta: Aricidea taylori (Pettibone, 1965) Cirrophorus lyra (Southern, 1914) Exogone lourei (Berkeley & Berkeley, 1938) Fabricinuda trilobata (Fitzhugh, 1990) Lumbrineris (Scoletoma) verrilli (Perkins, 1979) Syllis (Typosyllis) lutea (Harmann-Schroder, 1960) Gastropoda: Caecum pulchellum (Stimpson, 1851) Amphipoda: A. abdita Ampelisca holmesi (Pearse, 1908) Cerapus benthophilus (Thomas & Heard, 1979)
Average abundances in Florida Florida West Coast Bay
Average dissimilarity
0.015 0.440 0.123 12.869 1.726 2.797
9.402 22.065 8.348 47.114 11.255 10.674
0.797 1.035 0.645 0.655 0.704 0.602
9.254
31.799
0.621
34.581 7.765 22.728
0.522 0.000 4.375
0.741 0.623 0.593
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Figure 4. Results of cluster analysis of grid cells from the Gulf of Mexico coast using data from all salinity zones.
bott & Ladd, 1951) had higher average abundances in the Louisianian province than in the Florida west coast cluster. The last cluster included the rest of the original Louisianian province (grid cells, 259–266). Out of the entire region sampled, this cluster contained the majority of oligohaline and low mesohaline sites. Polyhaline or marine conditions dominated some grid cells while others represented estuarine systems that were almost exclusively oligohaline or mesohaline. Mud or muddy-sand sediments predominated this region and depths were mostly shallow (
