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Foraminiferal assemblage indices: A comparison of sediment and reef rubble samples from Conch Reef, Florida, USA
Ecological Indicators 48 (2015) 1–7
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Foraminiferal assemblage indices: A comparison of sediment and reef rubble samples from Conch Reef, Florida, USA Christy McNey Stephenson a , Pamela Hallock a,∗ , Francisco Kelmo b a b
College of Marine Science, University of South Florida, 830 1st Street South, St. Petersburg, FL 33701-5016, United States Instituto de Biologia, Universidade Federal da Bahia, Campus de Ondina, Salvador, Bahia CEP 40170-115, Brazil
a r t i c l e
i n f o
Article history: Received 17 June 2013 Received in revised form 2 July 2014 Accepted 3 July 2014 Keywords: Coral reefs Environmental indicators Foraminifera FORAM Index Biodiversity Diversity indices
a b s t r a c t Benthic foraminiferal assemblages are increasingly utilized as indicators of water and sediment quality in coastal-marine environments. Most reef-dwelling foraminifers live on firm substrata such as reef or phytal surfaces, while most assessments have examined assemblages from sediments. This case study compared relative abundances of total foraminiferal-shell assemblages between sediment and phytal/rubble samples collected from one reef within one week. A total of 117 species within 72 genera were identified, with the same taxa in both sample sets in different proportions. Larger benthic foraminifers and some agglutinated taxa were concentrated about 1.5–3 fold in sediment samples, while nearly twothirds of small, fragile shells were lost. Several common indices were compared, including Taxonomic Richness (number of genera), Shannon (H), Simpson’s (D) and Fisher (˛) diversity indices, Evenness (E), and the FORAM Index (FI). Highly significant differences (p < 0.001) between shell assemblages from 13 sets of phytal/rubble substrata and sediments were found in mean number (± standard deviation) of genera (49 ± 4 vs. 34 ± 10) and mean FI (5.6 ± 0.8 vs. 3.6 ± 0.4); both reflecting greater relative abundances of smaller foraminifers in the rubble samples. Fisher diversity was marginally significant (p = 0.05); other indices showed no significant differences between sample types. Although assessment of total assemblages is substantially less costly than distinguishing between specimens that were live or dead when collected, many researchers report those distinctions. The results of our study provide insight that can assist interpretations of studies that use live assemblages to calculate the FI, rather than total assemblages for which it was originally developed. © 2014 Elsevier Ltd. All rights reserved.
1. Introduction Foraminiferal assemblages have been used as environmental and paleoenvironmental indicators for more than 50 years. In reef environments, most motile benthic foraminifers live associated with “firm” substrata such as reef rock, crustose coralline algae, and many kinds of macroalgae, or within networks stabilized by filamentous algae, including algal mats. Nevertheless, most studies of reef-associated foraminiferal assemblages have assessed shells from reef sediments. Historically, when assemblages of reef foraminifers were studied for some combination of taxonomic assessment and to inform paleoenvironmental interpretation (e.g., Cushman et al., 1954; Rose and Lidz, 1977), bulk sediment samples were analyzed long after collection. Hallock (1981) demonstrated that algal symbiosis is a fundamental adaptation providing energetic benefit to calcareous
∗ Corresponding author. Tel.: +1 727 553 1567; fax: +1 727 553 1189. E-mail address: [email protected] (P. Hallock). http://dx.doi.org/10.1016/j.ecolind.2014.07.004 1470-160X/© 2014 Elsevier Ltd. All rights reserved.
organisms living in nutrient-poor environments. When the decline of coral reefs began to be recognized in the 1980s, Hallock (1988) noted that foraminiferal assemblages reflect whether environmental conditions are conducive to reef accretion. She subsequently proposed using foraminifers as indicators of reef health, formalizing that idea into a single-metric index of habitat suitability for calcifying organisms dependent upon algal symbioses (Hallock et al., 2003). The FORAM Index (FI) was based on the assumption that, if the environment supported active carbonate accretion, the shells of larger foraminifers, which hosted algal endosymbionts, should make up at least 25% of the total foraminiferal assemblage in reef sands (FI ≥ 4) (Hallock et al., 2003). If larger foraminiferal shells were present but made up less than 25% (2 < FI < 4), the environment was marginally suitable. If larger foraminifers were rare or absent (FI ≤ 2), the environment clearly was not suitable. Although differential sorting of larger and smaller foraminiferal shells was considered, the index was partly based on the observations of Cockey et al. (1996), who showed that proportions of larger foraminiferal shells had declined on decadal scales in
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C.M. Stephenson et al. / Ecological Indicators 48 (2015) 1–7
Fig. 1. Sampling sites in the vicinity of the Aquarius Underwater Habitat at Conch Reef in the Florida Keys National Marine Sanctuary.
Florida reef tract sediments consistent with overall reef decline and those proportions were not significantly dependent upon sediment texture. Although Hallock et al. (2003) assumed that some modification would have to be made to apply the FORAM Index outside the Caribbean/western North Atlantic region, the index has been successfully applied in Australia (e.g., Uthicke and Nobes, 2008; Fabricius et al., 2012) and elsewhere (see Hallock, 2012 and references therein). Several studies have applied the FORAM Index to live foraminiferal assemblages in reef sediments (e.g., Barbosa et al., 2009; Carilli and Walsh, 2012; Kelmo and Hallock, 2013). Such applications have often resulted in FI values between 3 and 4, even on reasonably healthy reefs. Since most taxa do not live in the sediments, we compared the assemblages associated with reef substrates upon which most foraminifers live, with assemblages from adjacent reef sediments, to see how closely the assemblages from the two substrates compared with respect to the FORAM Index and a variety of other common metrics. 2. Methods Thirteen sites at depths between 13 and 26 m were sampled in October 2008 in the vicinity of the Aquarius Habitat at Conch Reef, in the Florida Keys, USA (Fig. 1). Utilizing excursion-line intersections as sampling points, SCUBA divers haphazardly collected samples [i.e., with no a priori knowledge of what foraminifers might be found in any sample, e.g., Hayek and Buzas (2010)], which consisted of fist-sized pieces of reef rubble with associated microand macro-algae, into re-sealable plastic bags. Surface sediment samples were collected from adjacent sand patches into 30 ml vials. All samples were frozen to preserve color of foraminifers collected live (e.g., Hallock et al., 1986). Each sediment sample was thawed, placed into a 63 m mesh sieve fitted with a container to catch the mud fraction, and washed clean of muds. Both the mud and sand fractions were dried and weighed to determine weight-percent mud. The sand-sized fraction (>63 m) was divided using a sample splitter; one-half was
used in standard grain-size analysis and the other half examined microscopically to quantify the foraminiferal assemblages (#/g of sediment). All foraminiferal shells in good condition were removed from the sediment and placed on cardboard faunal slides. Each rubble sample was thawed, carefully scrubbed with a brush, and rinsed with fresh water to remove foraminifers and other meiofauna from the rock surface. Because many foraminifers adhered to algae or worm tubes, a sonicator was used to dislodge specimens attached to larger pieces. The resulting sample was dried and foraminiferal shells picked out and placed on cardboard faunal slides. The total seafloor area of each rubble piece was estimated from digital images so that numbers of foraminiferal shells/cm2 could be calculated (e.g., Baker et al., 2009). Foraminiferal shells were sorted and identified to genus using characteristics defined by Loeblich and Tappan (1987). For taxa that host algal symbionts, specimens collected live were readily distinguished by color and tabulated. To compile the species list for the samples, the faunal slides were examined and all species identified. For comparison of sand samples (#/g) with rubble samples (#/cm2 ), genus-level data were analyzed as relative abundances (i.e., proportions of the total sample examined). Genus-level accumulation curves were calculated for both data sets. Three sets of rubble samples and two sediment samples were collected at each sample site. Analysis of all of samples from four sites confirmed that variability could be as great between adjacent samples as between sites, so all samples processed were analyzed as discrete samples, although only one rubble sample and one sediment sample from the other nine sites were analyzed. For each sample, we calculated assemblage indices that are widely used in foraminiferal research: Taxonomic Richness (number of genera), Shannon (H), Fisher (˛), Simpson’s (D) diversity indices, and Evenness (E) (Hayek and Buzas, 2010). To calculate the FORAM Index (Hallock et al., 2003), the genera of foraminifers were tabulated in one of three functional categories based on their ecological roles in warm-water environments, i.e., symbiont-bearing taxa, stress-tolerant taxa, and other smaller taxa. T-tests were used to compare index means. Concentration ratios were calculated by
C.M. Stephenson et al. / Ecological Indicators 48 (2015) 1–7
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Table 1 Weight percent for each grain-size class for sediment samples from Conch Reef, October 2008. Grain size Site 2 3 5 5b 6 6b 7 10 11 12 13 15 15b 16 16b 17 18
>1 mm wt.%
1 mm wt.%
0.5 mm wt.%
0.25 mm wt.%
0.125 mm wt.%
0.063 mm wt.%
Mud wt.%
2.18 2.58 2.53 2.53 12.4 12.4 2.09 3.92 0.23 2.41 7.67 11.1 11.1 6.16 6.16 6.92 1.16
12.7 12.7 31.9 31.9 26.7 26.7 10.9 14.3 3.10 14.6 31.9 28.3 28.3 26.4 26.4 28.0 3.00
51.5 38.7 51.1 51.1 43.7 43.7 27.1 36.6 35.4 37.2 38.7 27.9 27.9 40.9 40.9 39.4 20.7
27.3 24.7 11.1 11.1 10.8 10.8 15.6 25.6 37.6 22.4 21.0 17.4 17.4 15.9 15.9 15.0 32.6
5.91 16.0 2.61 2.61 5.09 5.09 10.6 15.9 20.2 15.9 0.2 10.9 10.9 7.50 7.50 7.07 41.2
0.35 4.02 0.42 0.42 1.08 1.08 33.2 0.48 0.56 0.56 0.04 0.36 0.36 0.26 0.26 0.22 1.17
0.02 1.20 0.36 0.36 0.15 0.15 0.50 3.17 2.97 7.02 0.46 4.02 4.02 2.94 2.94 3.40 0.22
comparing the relative abundances of the 20 genera that were most common in both sample sets; each sediment abundance (S) was divided by the rubble abundance (R) to establish a ratio (S/R) for each genus. Multivariate analyses of foraminiferal assemblages followed Carnahan et al. (2009), assessing relative abundances of foraminifers from sediment and rubble samples to determine how sample sites grouped based on their similarity of assemblages (Q-mode analysis). Genera occurring in fewer than 5% of the samples were removed from the data set prior to analyses, consistent with recommended procedures (Clarke and Warwick, 2001; Parker and Arnold, 2002). PRIMERv6 (Plymouth Routines in Multivariate Ecological Research PRIMER-E Ltd., Plymouth) was used to construct Bray–Curtis similarity matrices on square-root transformed data. Based on this similarity matrix, we constructed a cluster dendrogram. 3. Results Grain-size analysis of the sediment samples revealed medium to coarse sand-sized sediments with less than 2% mud (Table 1). In all samples, a total of 117 species within 72 foraminiferal genera were identified (full data set can be found in Stephenson, 2011). No significant differences were found over the limited depth range sampled (mean depth 18 m). Most species belong to the order Miliolida (57 spp.), followed by Rotalida (34 spp.), and Bulminida (15 spp.). Only two genera, Reophax and Cibicoides, were found in sediment samples and not in the rubble; both were rare. Genera observed in the rubble but not in the sediment were Bolivinellina, Cassidulina, Floresina, Glabratella, Haynesina, Parahauerina, Reussella, Sigmavirgulina, Trochammina, and Valvulina; all were rare. Of the 62 foraminiferal genera within the sediment samples, the most abundant was Laevipeneroplis (11%), followed by Amphistegina (9%), Asterigerina and Quinqueloculina (8% each), and Archaias, Textularia, and Rosalina (5% each). Another 11 genera each accounted for at least 2% of the total, while 44 genera made up the remainder of the assemblage. Randomized genus-accumulation curves revealed that roughly 30 genera (half of those identified) can be found in nearly any sediment sample, but ∼10 samples are required to find 90% of the genera (Fig. 2). Of the 70 genera identified in the rubble samples, the dominant genus was Rosalina (9%), followed by Quinqueloculina and Planorbulina (8% each), Laevipeneroplis (7%), Miliolinella and Gavelinopsis (5% each). Genus-accumulation curves revealed that about two-thirds of the genera could be found in nearly any sample, and typically 90% of the genera could be found in five rubble samples (Fig. 2).
Assemblage indices (Tables 2–4) revealed more genera per sample in the rubble (49 ± 4.0) than in the sediment (34 ± 10). Fisher ˛ diversity was marginally higher (p = 0.05, n = 13) in rubble (12.9 ± 1.4) compared to the sediment samples (11.4 ± 2.3). Conversely, the FI was lower in the rubble samples (3.6 ± 0.4) than in the sediment (5.6 ± 0.8). Both indices reflect the greater abundance and variety of smaller foraminifers in the rubble samples. The Shannon Diversity (H), Simpson’s Diversity (D), and Evenness (E) indices did not differ significantly between the sample sets. Cluster analysis comparing the relative abundance data for sediment and rubble samples revealed three major clusters (Fig. 3), with 70% of the sediment samples clustering at greater than 60% similarity with the rubble samples; the remaining sediment samples were approximately 50% similar to all other samples. SIMPER analysis comparison of sediment and rubble samples revealed that sediment samples overall grouped at 65% similarity, with Laevipeneroplis, Amphistegina, Quinqueloculina, and Asterigerina, contributing most to the similarity. Rubble samples grouped together at 76% similarity with Rosalina, Quinqueloculina, Planorbulina, and Laevipeneroplis as the top four contributors. Sediment and rubble samples overall were 41% dissimilar with Planorbulina, Bolivina, Asterigerina, and Rosalina contributing most to the dissimilarity. The 20 genera that were most common in both sample sets (Table 5) included five symbiont-bearing taxa, along with one agglutinated textularid (Textularia) and one agglutinated miliolid (Siphonaptera), which were 2.7 times (median value) more
Fig. 2. Randomized accumulation plot for genera in sediment and reef-rubble samples from Conch Reef, October 2008.
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C.M. Stephenson et al. / Ecological Indicators 48 (2015) 1–7
Table 2 Summary of foraminiferal assemblage data and indices in all sediment samples assessed from Conch Reef, October 2008 (#/g = number per gram of sediment, #Gen = number of genera, SB = proportions of symbiont-bearing taxa, ST = proportions of stress-tolerant taxa, Other = proportions of other smaller taxa, FI = FORAM Index, ˛ = Fisher Diversity, H = Shannon Diversity, D = Simpson’s Diversity Index, E = Evenness Index, SD = standard deviation). Site
Depth (m)
#/g
#Gen
SB
ST
Other
FI
˛
H
D
E
2 3 5 5b 6 6b 7 10 11 12 13 15 15b 16 16b 17 18
20 20 13 13 13 13 20 14 17 20 18 25 25 26 26 17 20
157 401 38 41 85 110 236 286 425 678 51 301 402 239 326 274 555
30 35 14 16 21 31 35 35 36 45 24 38 46 40 50 39 36
0.60 0.49 0.68 0.60 0.36 0.32 0.45 0.44 0.43 0.28 0.54 0.40 0.32 0.41 0.43 0.45 0.44
0.03 0.03 0.03 0.00 0.00 0.02 0.02 0.02 0.01 0.03 0.04 0.07 0.03 0.03 0.06 0.03 0.02
0.37 0.48 0.29 0.40 0.64 0.67 0.54 0.54 0.56 0.69 0.42 0.54 0.65 0.56 0.51 0.52 0.54
6.8 5.9 7.4 6.8 4.9 4.5 5.5 5.5 5.4 4.2 6.3 5.1 4.5 5.2 5.4 5.5 5.5
8.9 11.2 8.0 9.4 8.3 12.2 11.3 10.7 10.8 14.7 8.1 11.3 13.4 12.7 16.0 13.6 12.8
2.8 3.0 2.4 2.6 2.4 3.1 2.8 2.9 3.1 3.3 2.8 3.1 3.3 3.0 3.3 3.2 3.1
0.92 0.94 0.91 0.94 0.86 0.95 0.91 0.92 0.97 0.95 0.93 0.95 0.96 0.94 0.95 0.95 0.96
0.53 0.58 0.77 0.83 0.51 0.70 0.46 0.52 0.62 0.57 0.67 0.60 0.60 0.52 0.56 0.60 0.62
Mean SD
18.8 2.1
271 178
33.6 9.8
0.45 0.11
0.03 0.02
0.52 0.11
5.6 0.8
11.4 2.3
2.9 0.3
0.93 0.03
0.60 0.09
Table 3 Summary of foraminiferal assemblage data and indices in all reef rubble samples assessed from Conch Reef, October 2008. (#Gen = number of genera, SB = symbiont-bearing taxa, ST = stress-tolerant taxa, Other = other smaller taxa, FI = FORAM Index, ˛ = Fisher Diversity, H = Shannon Diversity, D = Simpson’s Diversity Index, E = Evenness Index, SD = standard deviation). Site
Depth (m)
21 31 51 52 53 61 62 63 72 10 3 11 2 12 1 13 3 15 1 15 2 15 3 16 1 16 2 16 3 17 3 18 2
20 20 13 13 13 13 13 13 20 14 17 20 18 25 25 25 26 26 26 17 20
Mean SD
18.9 5.0
#/cm2 290 156 674 285 268 301 301 203 132 74 551 297 60 1116 534 1086 1059 1320 1094 644 198 507 390
# Gen
SB
ST
Other
FI
˛
H
D
E
47 48 45 45 49 49 49 49 50 48 54 55 45 43 51 50 54 53 57 54 42
0.23 0.25 0.17 0.17 0.18 0.17 0.19 0.22 0.22 0.20 0.13 0.18 0.25 0.22 0.21 0.20 0.24 0.22 0.16 0.18 0.39
0.03 0.06 0.06 0.07 0.08 0.05 0.06 0.10 0.10 0.05 0.13 0.11 0.06 0.06 0.04 0.06 0.05 0.07 0.07 0.05 0.02
0.74 0.69 0.77 0.76 0.74 0.79 0.75 0.69 0.68 0.75 0.73 0.71 0.69 0.71 0.75 0.75 0.71 0.72 0.78 0.77 0.59
3.8 3.9 3.3 3.3 3.4 3.3 3.4 3.6 3.6 3.6 2.9 3.3 3.9 3.7 3.6 3.5 3.9 3.7 3.2 3.4 5.1
8.2 12.9 12.3 13.3 15.0 12.1 11.7 13.0 12.7 13.7 13.5 13.1 12.5 11.5 14.7 13.0 15.2 13.5 13.1 12.3 13.8
3.3 3.2 3.2 3.3 3.2 3.2 3.1 3.1 3.1 3.2 3.1 3.1 3.1 3.2 2.4 2.7 2.6 2.5 3.2 2.0 2.7
0.95 0.95 0.95 0.95 0.95 0.95 0.93 0.94 0.95 0.95 0.95 0.96 0.95 0.95 0.93 0.96 0.95 0.95 0.95 0.93 0.91
0.64 0.67 0.64 0.68 0.63 0.61 0.57 0.63 0.73 0.68 0.64 0.54 0.72 0.71 0.27 0.33 0.31 0.30 0.57 0.16 0.57
49.4 4.0
0.21 0.05
0.07 0.03
0.73 0.04
3.6 0.4
12.9 1.4
3.0 0.3
0.94 0.01
0.55 0.17
abundant in sediments than in the rubble samples. Median S/R for smaller, more fragile taxa was 0.36, indicating that nearly twothirds of their shells were not represented in the sediment samples. In the sediment, representatives of four symbiont-bearing genera were recorded as alive when collected, based on color. In
the rubble, representatives of all nine common genera were found with symbiont color. Of the four taxa found live in both sample sets, Asterigerina and Peneroplis were found in similar percentages in both, while Laevipeneroplis was more than twice as likely to be found alive on rubble, and Amphistegina was 10
Table 4 Comparisons (t-statistic) of mean assemblage data and indices from sediment and rubble samples; means differ slightly from Tables 1 and 2 because data for sites where multiple samples were examined were combined so N = 13 and degrees of freedom = 12 for all t-tests. (#Genera = number of genera, SB = symbiont-bearing taxa, ST = stress-tolerant taxa, Other = other smaller taxa, FI = FORAM Index, ˛ = Fisher Diversity, H = Shannon Diversity, D = Simpson’s Diversity Index, E = Evenness Index, SD = standard deviation).
Sediment (mean) Sediment (SD) Rubble (mean) Rubble (SD) T-statistic Probability
# Genera
SB
ST
34.1 8.58 49.40 4.00 −7.06 1.3E−05
0.45 0.10 0.22 0.061 7.80 4.9E−06
0.026 0.012 0.068 0.031 −4.16 0.0013
Other 0.52 0.10 0.72 0.047 −6.15 5E−05
FI
˛
H
D
E
5.6 0.8 3.6 0.4 7.90 4.3E−06
11.4 2.12 12.9 1.41 −2.20 0.05
2.96 0.23 2.97 0.34 −0.23 0.83
0.94 0.02 0.94 0.01 −1.22 0.25
0.59 0.08 0.55 0.17 0.19 0.85
C.M. Stephenson et al. / Ecological Indicators 48 (2015) 1–7
Fig. 3. Cluster analysis (Bray–Curtis similarity) of square-root transformed, percentabundance data for foraminiferal assemblages from the sediment and rubble samples (#, # and #* indicate multiple samples from the same site).
times more likely to be collected live from rubble than from sand. 4. Discussion Foraminiferal assemblages of the Florida reef tract are well known (e.g., Bock, 1971; Culver and Buzas, 1982). Lidz and Rose (1989), working only with sediment samples from Florida, reported ∼50 foraminiferal species representing 32 genera and 20 families. Wright and Hay (1971) found 117 species representing 60 genera from the Florida reef tract. Both data sets included a wider range of environments than our data set from a single shelf-margin reef. The primary differences between our taxonomic list and previous studies were in recent generic distinctions, following Loeblich and Tappan (1987). Nevertheless, our results showed that the benthic foraminiferal assemblage on the Florida reef tract is well known, very diverse, and well represented even at a single reef location. Moreover, the genus accumulation curves revealed that a single
Table 5 Relative abundances of the 20 most common genera used to calculate a concentration ratio (S/R) for each genus. Genus
Sediment
Rubble
S/R
Amphistegina Archaias Articulina Asterigerina Bolivina Borelis Cibicides Cyclorbiculina Discorbis Gavelinopsis Laevipeneroplis Miliolinella Neoconorbina Planorbulina Pseudoschlumbergerina Pseudotriloculina Quinqueloculina Rosalina Siphonapteraa Textulariab
9.37 5.45 2.68 8.34 0.21 2.50 0.41 3.96 3.70 1.68 11.4 1.87 0.80 1.79 2.01 1.35 8.09 5.11 2.83 5.43
3.76 1.97 2.23 2.85 3.10 0.91 2.48 0.71 1.95 4.66 7.14 5.25 3.24 8.10 4.02 3.04 8.17 8.85 0.57 2.11
2.50 2.77 1.21 2.92 0.07 2.73 0.16 5.55 1.90 0.36 1.60 0.36 0.25 0.22 0.50 0.44 0.99 0.58 5.01 2.57
a b
Agglutinated miliolid. Agglutinated textularid.
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sample is likely to recover at least half the common genera and that three samples are likely to recover about two-thirds of them. The samples overall were quite homogenous. The primary differences between sample types were in the relative abundances of smaller foraminifers. In both sample sets, more than 70% of the genera occurred at 1% abundance or less. The 12 genera not found in both sample types were uncommon, occurring in only one or two samples overall. Thus, the sediment assemblages, which were mostly dead shells, generally reflected the taxa living on the rubble/phytal substrates in the area, although not their proportions. More taxa were found in the rubble samples than in the sediment samples; smaller, more fragile taxa were clearly underrepresented in the sediments. Nevertheless, most of the sediment samples clustered with the rubble samples at greater than 60% similarity. This was actually somewhat surprising given the coarse texture of the sediments. Concentration ratios quantified the observation that the more robust taxa tend to be concentrated in the sediments compared to smaller and more delicate taxa. Amphistegina, Archaias, Asterigerina, Borelis, and Laevipeneroplis all exhibited ratios between approximately 1.5 and 3. Cyclorbiculina had the highest concentration ratio of the symbiont-bearing taxa; possibly an artifact of its larger, wingshaped structure, which may enhance transport of the shells from shallower environments (Hohenegger et al., 1999). Archaias, a similar symbiont-bearing Miliolida, has robust shells that are thick and reinforced by pillars, which allows the shells to be resistant to abrasion and winnowing and therefore to accumulate in carbonate sediments (Martin, 1986). The distributions of Asterigerina were notable. These foraminifers have intermediate-sized shells, are thick-walled, biconvex in shape, and host algal symbionts. The shells and even living specimens were found commonly in both sediment and rubble samples. Previous studies have noted the abundance of this species, and of the robust but smaller Discorbis rosea, in high-energy reef environments (Crevison et al., 2006; Ramirez, 2008; Baker et al., 2009). Besides D. rosea, two other smaller genera were found more than twice as commonly in sediment as on rubble. Siphonaptera, an agglutinated miliolid, was approximately five times more common, while Textularia, which belongs to the agglutinate Order Textularida, was about 2.5 times more common in sediment. Whether these differences indicate that the taxa live in sediments or are simply more resistant to destruction is not known, but one can speculate on both possibilities. In the first, sediment particles with which to build an agglutinated shell are more readily available to foraminifers living in the sediments. Siphonaptera was previously reported (Carnahan et al., 2009) to cluster with symbiont-bearing foraminifers that are indicative of oligotrophic environments. Two smaller miliolid genera, Articulina and Quinqueloculina, were found similarly represented in sediment and rubble samples (Table 5). Both genera are relatively diverse and some species in both genera have intermediate-sized, relatively thick shells. Again, members of these genera may be living in the sediment as commonly as on rubble, and those with relatively thick shells would have higher preservation potential (Boltovskoy and Wright, 1976; Wetmore, 1987). Previous studies comparing live and dead assemblages have commonly reported that living foraminifers are seldom abundant in sediment samples, and that diversities are higher in dead assemblages (e.g., Lynts, 1966; Scott and Medioli, 1980; Alve, 2000). Buzas et al. (2002) found that dead assemblages reflect the overall environment, while the live assemblage in any given sample may reveal a local bloom. Murray and Alve (2000) reported that substantial spatial variation can occur within a centimeter and that dead assemblages represent the time-averaged contribution of empty shells from the production of successive living assemblages, with
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modification by postmortem processes. Studies comparing live and dead assemblages in reef-sediment samples (e.g., Cockey et al., 1996; Peebles et al., 1997) reported that foraminifers collected alive typically made up less than 10% of the foraminiferal shells identified. Our results reported here are consistent with such previous reports. Comparing live and dead assemblages was not a primary goal of our study as the samples we evaluated were not stained. Nevertheless, protoplasm color allowed symbiont-bearing taxa collected live to be easily distinguished from dead shells. The highest percentages of specimens collected live in sediments were 6% for Asterigerina and Laevipeneroplis. Amphistegina was about 10 times more likely to be found alive in the rubble samples than in the adjacent sediments. Similarly, Martin (1986) found Archaias living primarily on vegetation, with virtually no living Archaias in his sediment samples. We found neither Archaias nor Cyclorbiculina collected alive in sediment samples, though dead shells of both were common. Because these taxa have relatively large shells that are resistant to destruction, their dead shells are often abundant in the shelf sediments of the tropical western Atlantic and Caribbean (Martin, 1986; Triffleman et al., 1991; Peebles et al., 1997; many others). The FORAM Index (FI) was developed to reflect the response of the calcifying benthic community to the suitability of the environment for reef growth (Hallock et al., 2003). In our samples, the mean FI of sediment samples was 5.6 ± 0.8, indicating that the water quality at Conch Reef was suitable for accretion. The FI was developed using total assemblages from sediment samples because their collection adds minimal time to a field sampling effort. Moreover, collection of sediment samples for analysis of total assemblages does not require transport of preservatives, minimizing logistical considerations, as well as costs of collection and transport to the laboratory (Hallock et al., 2003). Some researchers have applied the FI to live reef assemblages (e.g., Barbosa et al., 2009; Koukousioura et al., 2011; Carilli and Walsh, 2012; Kelmo and Hallock, 2013), often yielding values in the 3–4 range. Our data set provided the opportunity to compare the FI values from rubble substrata, which more closely represented the live assemblage, and from the total assemblage from sediments. The mean FI for the rubble samples was lower, 3.6 ± 0.4; but still indicating a significant contribution by symbiont-bearing foraminifers, consistent with the assessment that water quality at Conch Reef supports calcifying symbioses. No significant differences were found between the means of other indices calculated (Shannon Diversity, Simpson’s Diversity, and Evenness) for sediment and rubble samples (Table 4); only FI, the number of genera per sample, and the Fisher ˛ exhibited differences. Hayek and Buzas (2010) recommended the use of the diversity and evenness indices for assessing assemblages, so the fact that those indices did not reveal significant differences between our rubble and sediment samples indicates the robustness of analyses based on total assemblages in reef environments. While taxonomic richness was higher in the rubble samples, when standardized to sample size using the Fisher ˛ index, the difference between the sediment and rubble samples was only marginally significant. In conclusion, the sediment reveals what taxa have been living in an area in the recent past and that are present at the time of sampling. The underlying observation for the FORAM Index is that sediments on healthy reefs have a larger proportion of shells of symbiont-bearing foraminifers compared to other smaller foraminifers and stress-tolerant foraminifers (Hallock, 1988; Hallock et al., 2003). Foraminifers found in the sediments are represented primarily by empty shells, while live specimens can be found living on a variety of substrates. According to Engle (2000, p. 3-1), “an ideal indicator of the response of benthic organisms to perturbations in the environment would not only quantify
their present condition in the ecosystems but would also integrate the effects of anthropogenic and natural stressors on the organisms over time”. “This information is precisely what foraminiferal shells in the sediments can provide” (Hallock et al., 2003, p. 223). Acknowledgments Field support was provided through NOAA contract number to NURC-UNCW: NA080AR4300863; subcontract to UNC-Chapel Hill: ARB-2008-11 (PIs: C. Martens and N. Lindquist); subcontract to USF: 5-46147 (PIs: P. Hallock Muller and R. Byrne). J. Scott Fulcher provided assistance in processing samples. Kendra Daly, Lisa Robbins, and anonymous reviewers provided comments that improved the manuscript. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.ecolind. 2014.07.004. These data include Google maps of the most important areas described in this article. References Alve, E., 2000. Environmental stratigraphy: a case study reconstructing bottom water oxygen conditions in Frierfjord, Norway, over the past five centuries. In: Martin, R.E. (Ed.), Environmental Micropaleontology. Kluwer Academic/Plenum Publishers, Boston, pp. 324–350. Baker, R.D., Hallock, P., Moses, E.F., Williams, D.E., Ramirez, A., 2009. Larger foraminifers of the Florida Reef Tract, USA: distribution patterns on reef-rubble habitats. J. Foraminifer. Res. 39, 267–277. Barbosa, C.F., Prazeres, M., de Freitas, Ferreira, B.P., Seoane, J.C.S., 2009. Foraminiferal assemblage and reef check census in coral reef health monitoring of East Brazilian margin. Mar. Micropaleontol. 73, 62–69. Bock, W.D., 1971. A handbook of benthic Foraminifera of Florida Bay and adjacent waters. In: Jones, J.I., Bock, W.D. (Eds.), A Symposium of Recent South Florida Foraminifera, vol. 1. Miami Geol. Soc. Mem., Miami, FL, pp. 1–72. Boltovskoy, E., Wright, R., 1976. Recent Foraminifera. Junk, The Hague. Buzas, M.A., Hayek, L.C., Reed, S.A., Jett, J.A., 2002. Foraminiferal densities over five years in the Indian River Lagoon, Florida: a model of pulsating patches. J. Foraminifer. Res. 32, 68–93. Carilli, J., Walsh, S., 2012. Benthic foraminiferal assemblages from Kiritimati (Christmas) Island indicate human-mediated nitrification has occurred over the scale of decades. Mar. Ecol. Prog. Ser. 456, 87–99. Carnahan, E.A., Hoare, A.M., Hallock, P., Lidz, B.H., Reich, C.D., 2009. Foraminiferal assemblages in Biscayne Bay, Florida USA: responses to urban and agricultural influence in a subtropical Estuary. Mar. Pollut. Bull. 59, 221–233. Clarke, K.R., Warwick, R.M., 2001. Changes in Marine Communities: An Approach to Statistical Analysis and Interpretations. PRIMER-E Ltd., Plymouth Marine Laboratory, UK, www.PRIMER-e.com Cockey, E., Hallock, P., Lidz, B.H., 1996. Decadal scale changes in benthic foraminiferal assemblages off Key Largo, Florida. Coral Reefs 15, 237–248. Crevison, H., Hallock, P., McRae, G., 2006. Sediment cores from the Florida Keys Reef Tract (USA): is resolution sufficient for environmental applications? JEMMM 3, 61–82. Culver, S.J., Buzas, M.A., 1982. Distribution of recent benthic Foraminifera in the Caribbean Region. Smithsonian Contrib. Mar. Sci. 14, 1–382. Cushman, J.A., Todd, R., Post, R., 1954. Recent Foraminifera of the Marshall Islands, Bikini and nearby atolls. 2. Oceanography (biology). U.S. Geol. Surv. Prof. Pap. 260-II, 319–384. Engle, V.D., 2000. Application of the indicator evaluation guidelines to an index of benthic condition for Gulf of Mexico estuaries. In: Jackson, L.E., Kurtz, J.C., Fisher, W.S. (Eds.), Evaluation Guidelines for Ecological Indicators. EPA/620/R-99/005, vol. 3. U.S. Environmental Protection Agency, Research Triangle Park, Durham, NC, pp. 1–29. Fabricius, K.E., Cooper, T.F., Humphrey, C., Uthicke, S., De’ath, G., Davidson, J., LeGrand, H., Thompson, A., Schaffelke, B., 2012. A bioindicator system for water quality on inshore coral reefs of the Great Barrier Reef. Mar. Pollut. Bull. 65 (SI), 320–332. Hallock, P., 1981. Algal symbiosis: a mathematical analysis. Mar. Biol. 62, 249–255. Hallock, P., 1988. The role of nutrient availability in bioerosion: consequences to carbonate buildup. Palaeogeogr. Palaeoclimatol. Palaeoecol. 63, 275–291. Hallock, P., 2012. The FORAM Index revisited: usefulness, challenges and limitations. In: Proceedings of the International Coral Reef Symposium, Cairns, Australia, 9–13 July 2012, http://www.icrs2012.com/proceedings/ manuscripts/ICRS2012 15F 2.pdf Hallock, P., Cottey, T.L., Forward, L.B., Halas, J., 1986. Population biology and sediment production of Archaias angulatus (Foraminiferida) in Largo Sound, Florida. J. Foraminifer. Res. 16, 1–8.
C.M. Stephenson et al. / Ecological Indicators 48 (2015) 1–7 Hallock, P., Lidz, B.H., Cockey-Burkhard, E.M., Donnelly, K.B., 2003. Foraminifera as bioindicators in coral reef assessment and monitoring: the FORAM Index. Environ. Monit. Assess. 81, 221–238. Hayek, L.C., Buzas, M.A., 2010. Surveying Natural Populations: Quantitative Tools for Assessing Biodiversity. Columbia University Press, New York. Hohenegger, J., Yordanova, E., Nakano, Y., Tatazreiter, F., 1999. Habitats of larger Foraminifera on the upper reef slope of Sesoko Island, Okinawa Japan. Mar. Micropaleontol. 36, 109–168. Kelmo, F., Hallock, P., 2013. Responses of foraminiferal assemblages to ENSO climate patterns on bank reefs of northern Bahia, Brazil: a 17-year record. Ecol. Indic. 30, 148–157, http://dx.doi.org/10.1016/j.ecolind.2013.02.009. Koukousioura, O., Dimiza, M.D., Triantaphyllou, M.V., Hallock, P., 2011. Living benthic foraminifera as an environmental proxy in coastal ecosystems: a case study from the Aegean Sea (Greece, NE Mediterranean). J. Mar. Syst. 88, 489–501. Lidz, B.H., Rose, P.R., 1989. Diagnostic foraminiferal assemblages of Florida Bay and adjacent shallow waters: a comparison. Bull. Mar. Sci. 44, 399–418. Loeblich Jr., A.R., Tappan, H., 1987. Foraminiferal Genera and their Classification. Van Nostrand Reinhold, New York. Lynts, G.W., 1966. Variation of foraminiferal standing crop over short distances in Buttonwood Sound, Florida Bay. Limnol. Oceanogr. 11, 562–566. Martin, R.E., 1986. Habitat and distribution of the foraminifer Archaias angulatus (Fitchel and Moll) (Miliolida, Soritidae) Northern Florida Keys. J. Foraminifer. Res. 16, 201–206. Murray, J.W., Alve, E., 2000. Major aspects of foraminiferal variability (standing crop and biomass) on a monthly scale in an intertidal zone. J. Foraminifer. Res. 30, 177–191. Parker, W.C., Arnold, A.J., 2002. Quantitative methods in data analysis in foraminiferal ecology. In: Sen Gupta, B. (Ed.), Modern Foraminifera. Kluwer Academic Publisher, Dordrecht, pp. 71–89.
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Peebles, M.W., Hallock, P., Hine, A.C., 1997. Benthic foraminiferal assemblages from current-swept carbonate platforms of the northern Nicaraguan Rise, Caribbean Sea. J. Foraminifer. Res. 27, 42–50. Ramirez, A., (MS thesis) 2008. Patch Reef Health in Biscayne National Park: A Comparison of Three Foraminiferal Indices. University of South Florida, Tampa, FL (unpublished). http://scholarcommons.usf.edu/cgi/viewcontent. cgi?article=1464&context=etd Rose, P.R., Lidz, B.H., 1977. Diagnostic foraminiferal assemblages of shallow-water modern environments: South Florida and the Bahamas. Sedimentia 1, 1–56. Scott, D.B., Medioli, F.S., 1980. Total foraminiferal populations: their relative usefulness in paleoecology. J. Paleontol. 54, 814–831. Stephenson, C.M., (MS thesis) 2011. Foraminiferal Assemblages on Sediments and Reef Rubble at Conch Reef, Florida, USA. University of South Florida, Tampa, FL (unpublished). http://scholarcommons.usf.edu/cgi/viewcontent. cgi?article=4562&context=etd Triffleman, N.J., Hallock, P., Hine, A.C., Peebles, M., 1991. Distribution of foraminiferal tests in sediments of Serranilla Bank, Nicaraguan Rise, southwestern Caribbean. J. Foraminifer. Res. 21, 39–47. Uthicke, S., Nobes, K., 2008. Benthic Foraminifera as ecological indicators for water quality on the Great Barrier Reef. Estuar. Coast. Shelf Sci. 78, 763–773. Wetmore, K.L., 1987. Correlations between test strength, morphology, and habitat in some benthic Foraminifera from the coast of Washington. J. Foraminifer. Res. 17, 1–13. Wright, R.C., Hay, W.W., 1971. The abundance and distribution of foraminifers in a back-reef environment, Molasses Reef, Florida. In: Jones, J.I., Bock, W.D. (Eds.), A Symposium of Recent South Florida Foraminifera, vol. 1. Miami Geol. Soc. Mem., Miami, FL, pp. 121–174.
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Ecological Indicators journal homepage: www.elsevier.com/locate/ecolind
Foraminiferal assemblage indices: A comparison of sediment and reef rubble samples from Conch Reef, Florida, USA Christy McNey Stephenson a , Pamela Hallock a,∗ , Francisco Kelmo b a b
College of Marine Science, University of South Florida, 830 1st Street South, St. Petersburg, FL 33701-5016, United States Instituto de Biologia, Universidade Federal da Bahia, Campus de Ondina, Salvador, Bahia CEP 40170-115, Brazil
a r t i c l e
i n f o
Article history: Received 17 June 2013 Received in revised form 2 July 2014 Accepted 3 July 2014 Keywords: Coral reefs Environmental indicators Foraminifera FORAM Index Biodiversity Diversity indices
a b s t r a c t Benthic foraminiferal assemblages are increasingly utilized as indicators of water and sediment quality in coastal-marine environments. Most reef-dwelling foraminifers live on firm substrata such as reef or phytal surfaces, while most assessments have examined assemblages from sediments. This case study compared relative abundances of total foraminiferal-shell assemblages between sediment and phytal/rubble samples collected from one reef within one week. A total of 117 species within 72 genera were identified, with the same taxa in both sample sets in different proportions. Larger benthic foraminifers and some agglutinated taxa were concentrated about 1.5–3 fold in sediment samples, while nearly twothirds of small, fragile shells were lost. Several common indices were compared, including Taxonomic Richness (number of genera), Shannon (H), Simpson’s (D) and Fisher (˛) diversity indices, Evenness (E), and the FORAM Index (FI). Highly significant differences (p < 0.001) between shell assemblages from 13 sets of phytal/rubble substrata and sediments were found in mean number (± standard deviation) of genera (49 ± 4 vs. 34 ± 10) and mean FI (5.6 ± 0.8 vs. 3.6 ± 0.4); both reflecting greater relative abundances of smaller foraminifers in the rubble samples. Fisher diversity was marginally significant (p = 0.05); other indices showed no significant differences between sample types. Although assessment of total assemblages is substantially less costly than distinguishing between specimens that were live or dead when collected, many researchers report those distinctions. The results of our study provide insight that can assist interpretations of studies that use live assemblages to calculate the FI, rather than total assemblages for which it was originally developed. © 2014 Elsevier Ltd. All rights reserved.
1. Introduction Foraminiferal assemblages have been used as environmental and paleoenvironmental indicators for more than 50 years. In reef environments, most motile benthic foraminifers live associated with “firm” substrata such as reef rock, crustose coralline algae, and many kinds of macroalgae, or within networks stabilized by filamentous algae, including algal mats. Nevertheless, most studies of reef-associated foraminiferal assemblages have assessed shells from reef sediments. Historically, when assemblages of reef foraminifers were studied for some combination of taxonomic assessment and to inform paleoenvironmental interpretation (e.g., Cushman et al., 1954; Rose and Lidz, 1977), bulk sediment samples were analyzed long after collection. Hallock (1981) demonstrated that algal symbiosis is a fundamental adaptation providing energetic benefit to calcareous
∗ Corresponding author. Tel.: +1 727 553 1567; fax: +1 727 553 1189. E-mail address: [email protected] (P. Hallock). http://dx.doi.org/10.1016/j.ecolind.2014.07.004 1470-160X/© 2014 Elsevier Ltd. All rights reserved.
organisms living in nutrient-poor environments. When the decline of coral reefs began to be recognized in the 1980s, Hallock (1988) noted that foraminiferal assemblages reflect whether environmental conditions are conducive to reef accretion. She subsequently proposed using foraminifers as indicators of reef health, formalizing that idea into a single-metric index of habitat suitability for calcifying organisms dependent upon algal symbioses (Hallock et al., 2003). The FORAM Index (FI) was based on the assumption that, if the environment supported active carbonate accretion, the shells of larger foraminifers, which hosted algal endosymbionts, should make up at least 25% of the total foraminiferal assemblage in reef sands (FI ≥ 4) (Hallock et al., 2003). If larger foraminiferal shells were present but made up less than 25% (2 < FI < 4), the environment was marginally suitable. If larger foraminifers were rare or absent (FI ≤ 2), the environment clearly was not suitable. Although differential sorting of larger and smaller foraminiferal shells was considered, the index was partly based on the observations of Cockey et al. (1996), who showed that proportions of larger foraminiferal shells had declined on decadal scales in
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C.M. Stephenson et al. / Ecological Indicators 48 (2015) 1–7
Fig. 1. Sampling sites in the vicinity of the Aquarius Underwater Habitat at Conch Reef in the Florida Keys National Marine Sanctuary.
Florida reef tract sediments consistent with overall reef decline and those proportions were not significantly dependent upon sediment texture. Although Hallock et al. (2003) assumed that some modification would have to be made to apply the FORAM Index outside the Caribbean/western North Atlantic region, the index has been successfully applied in Australia (e.g., Uthicke and Nobes, 2008; Fabricius et al., 2012) and elsewhere (see Hallock, 2012 and references therein). Several studies have applied the FORAM Index to live foraminiferal assemblages in reef sediments (e.g., Barbosa et al., 2009; Carilli and Walsh, 2012; Kelmo and Hallock, 2013). Such applications have often resulted in FI values between 3 and 4, even on reasonably healthy reefs. Since most taxa do not live in the sediments, we compared the assemblages associated with reef substrates upon which most foraminifers live, with assemblages from adjacent reef sediments, to see how closely the assemblages from the two substrates compared with respect to the FORAM Index and a variety of other common metrics. 2. Methods Thirteen sites at depths between 13 and 26 m were sampled in October 2008 in the vicinity of the Aquarius Habitat at Conch Reef, in the Florida Keys, USA (Fig. 1). Utilizing excursion-line intersections as sampling points, SCUBA divers haphazardly collected samples [i.e., with no a priori knowledge of what foraminifers might be found in any sample, e.g., Hayek and Buzas (2010)], which consisted of fist-sized pieces of reef rubble with associated microand macro-algae, into re-sealable plastic bags. Surface sediment samples were collected from adjacent sand patches into 30 ml vials. All samples were frozen to preserve color of foraminifers collected live (e.g., Hallock et al., 1986). Each sediment sample was thawed, placed into a 63 m mesh sieve fitted with a container to catch the mud fraction, and washed clean of muds. Both the mud and sand fractions were dried and weighed to determine weight-percent mud. The sand-sized fraction (>63 m) was divided using a sample splitter; one-half was
used in standard grain-size analysis and the other half examined microscopically to quantify the foraminiferal assemblages (#/g of sediment). All foraminiferal shells in good condition were removed from the sediment and placed on cardboard faunal slides. Each rubble sample was thawed, carefully scrubbed with a brush, and rinsed with fresh water to remove foraminifers and other meiofauna from the rock surface. Because many foraminifers adhered to algae or worm tubes, a sonicator was used to dislodge specimens attached to larger pieces. The resulting sample was dried and foraminiferal shells picked out and placed on cardboard faunal slides. The total seafloor area of each rubble piece was estimated from digital images so that numbers of foraminiferal shells/cm2 could be calculated (e.g., Baker et al., 2009). Foraminiferal shells were sorted and identified to genus using characteristics defined by Loeblich and Tappan (1987). For taxa that host algal symbionts, specimens collected live were readily distinguished by color and tabulated. To compile the species list for the samples, the faunal slides were examined and all species identified. For comparison of sand samples (#/g) with rubble samples (#/cm2 ), genus-level data were analyzed as relative abundances (i.e., proportions of the total sample examined). Genus-level accumulation curves were calculated for both data sets. Three sets of rubble samples and two sediment samples were collected at each sample site. Analysis of all of samples from four sites confirmed that variability could be as great between adjacent samples as between sites, so all samples processed were analyzed as discrete samples, although only one rubble sample and one sediment sample from the other nine sites were analyzed. For each sample, we calculated assemblage indices that are widely used in foraminiferal research: Taxonomic Richness (number of genera), Shannon (H), Fisher (˛), Simpson’s (D) diversity indices, and Evenness (E) (Hayek and Buzas, 2010). To calculate the FORAM Index (Hallock et al., 2003), the genera of foraminifers were tabulated in one of three functional categories based on their ecological roles in warm-water environments, i.e., symbiont-bearing taxa, stress-tolerant taxa, and other smaller taxa. T-tests were used to compare index means. Concentration ratios were calculated by
C.M. Stephenson et al. / Ecological Indicators 48 (2015) 1–7
3
Table 1 Weight percent for each grain-size class for sediment samples from Conch Reef, October 2008. Grain size Site 2 3 5 5b 6 6b 7 10 11 12 13 15 15b 16 16b 17 18
>1 mm wt.%
1 mm wt.%
0.5 mm wt.%
0.25 mm wt.%
0.125 mm wt.%
0.063 mm wt.%
Mud wt.%
2.18 2.58 2.53 2.53 12.4 12.4 2.09 3.92 0.23 2.41 7.67 11.1 11.1 6.16 6.16 6.92 1.16
12.7 12.7 31.9 31.9 26.7 26.7 10.9 14.3 3.10 14.6 31.9 28.3 28.3 26.4 26.4 28.0 3.00
51.5 38.7 51.1 51.1 43.7 43.7 27.1 36.6 35.4 37.2 38.7 27.9 27.9 40.9 40.9 39.4 20.7
27.3 24.7 11.1 11.1 10.8 10.8 15.6 25.6 37.6 22.4 21.0 17.4 17.4 15.9 15.9 15.0 32.6
5.91 16.0 2.61 2.61 5.09 5.09 10.6 15.9 20.2 15.9 0.2 10.9 10.9 7.50 7.50 7.07 41.2
0.35 4.02 0.42 0.42 1.08 1.08 33.2 0.48 0.56 0.56 0.04 0.36 0.36 0.26 0.26 0.22 1.17
0.02 1.20 0.36 0.36 0.15 0.15 0.50 3.17 2.97 7.02 0.46 4.02 4.02 2.94 2.94 3.40 0.22
comparing the relative abundances of the 20 genera that were most common in both sample sets; each sediment abundance (S) was divided by the rubble abundance (R) to establish a ratio (S/R) for each genus. Multivariate analyses of foraminiferal assemblages followed Carnahan et al. (2009), assessing relative abundances of foraminifers from sediment and rubble samples to determine how sample sites grouped based on their similarity of assemblages (Q-mode analysis). Genera occurring in fewer than 5% of the samples were removed from the data set prior to analyses, consistent with recommended procedures (Clarke and Warwick, 2001; Parker and Arnold, 2002). PRIMERv6 (Plymouth Routines in Multivariate Ecological Research PRIMER-E Ltd., Plymouth) was used to construct Bray–Curtis similarity matrices on square-root transformed data. Based on this similarity matrix, we constructed a cluster dendrogram. 3. Results Grain-size analysis of the sediment samples revealed medium to coarse sand-sized sediments with less than 2% mud (Table 1). In all samples, a total of 117 species within 72 foraminiferal genera were identified (full data set can be found in Stephenson, 2011). No significant differences were found over the limited depth range sampled (mean depth 18 m). Most species belong to the order Miliolida (57 spp.), followed by Rotalida (34 spp.), and Bulminida (15 spp.). Only two genera, Reophax and Cibicoides, were found in sediment samples and not in the rubble; both were rare. Genera observed in the rubble but not in the sediment were Bolivinellina, Cassidulina, Floresina, Glabratella, Haynesina, Parahauerina, Reussella, Sigmavirgulina, Trochammina, and Valvulina; all were rare. Of the 62 foraminiferal genera within the sediment samples, the most abundant was Laevipeneroplis (11%), followed by Amphistegina (9%), Asterigerina and Quinqueloculina (8% each), and Archaias, Textularia, and Rosalina (5% each). Another 11 genera each accounted for at least 2% of the total, while 44 genera made up the remainder of the assemblage. Randomized genus-accumulation curves revealed that roughly 30 genera (half of those identified) can be found in nearly any sediment sample, but ∼10 samples are required to find 90% of the genera (Fig. 2). Of the 70 genera identified in the rubble samples, the dominant genus was Rosalina (9%), followed by Quinqueloculina and Planorbulina (8% each), Laevipeneroplis (7%), Miliolinella and Gavelinopsis (5% each). Genus-accumulation curves revealed that about two-thirds of the genera could be found in nearly any sample, and typically 90% of the genera could be found in five rubble samples (Fig. 2).
Assemblage indices (Tables 2–4) revealed more genera per sample in the rubble (49 ± 4.0) than in the sediment (34 ± 10). Fisher ˛ diversity was marginally higher (p = 0.05, n = 13) in rubble (12.9 ± 1.4) compared to the sediment samples (11.4 ± 2.3). Conversely, the FI was lower in the rubble samples (3.6 ± 0.4) than in the sediment (5.6 ± 0.8). Both indices reflect the greater abundance and variety of smaller foraminifers in the rubble samples. The Shannon Diversity (H), Simpson’s Diversity (D), and Evenness (E) indices did not differ significantly between the sample sets. Cluster analysis comparing the relative abundance data for sediment and rubble samples revealed three major clusters (Fig. 3), with 70% of the sediment samples clustering at greater than 60% similarity with the rubble samples; the remaining sediment samples were approximately 50% similar to all other samples. SIMPER analysis comparison of sediment and rubble samples revealed that sediment samples overall grouped at 65% similarity, with Laevipeneroplis, Amphistegina, Quinqueloculina, and Asterigerina, contributing most to the similarity. Rubble samples grouped together at 76% similarity with Rosalina, Quinqueloculina, Planorbulina, and Laevipeneroplis as the top four contributors. Sediment and rubble samples overall were 41% dissimilar with Planorbulina, Bolivina, Asterigerina, and Rosalina contributing most to the dissimilarity. The 20 genera that were most common in both sample sets (Table 5) included five symbiont-bearing taxa, along with one agglutinated textularid (Textularia) and one agglutinated miliolid (Siphonaptera), which were 2.7 times (median value) more
Fig. 2. Randomized accumulation plot for genera in sediment and reef-rubble samples from Conch Reef, October 2008.
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C.M. Stephenson et al. / Ecological Indicators 48 (2015) 1–7
Table 2 Summary of foraminiferal assemblage data and indices in all sediment samples assessed from Conch Reef, October 2008 (#/g = number per gram of sediment, #Gen = number of genera, SB = proportions of symbiont-bearing taxa, ST = proportions of stress-tolerant taxa, Other = proportions of other smaller taxa, FI = FORAM Index, ˛ = Fisher Diversity, H = Shannon Diversity, D = Simpson’s Diversity Index, E = Evenness Index, SD = standard deviation). Site
Depth (m)
#/g
#Gen
SB
ST
Other
FI
˛
H
D
E
2 3 5 5b 6 6b 7 10 11 12 13 15 15b 16 16b 17 18
20 20 13 13 13 13 20 14 17 20 18 25 25 26 26 17 20
157 401 38 41 85 110 236 286 425 678 51 301 402 239 326 274 555
30 35 14 16 21 31 35 35 36 45 24 38 46 40 50 39 36
0.60 0.49 0.68 0.60 0.36 0.32 0.45 0.44 0.43 0.28 0.54 0.40 0.32 0.41 0.43 0.45 0.44
0.03 0.03 0.03 0.00 0.00 0.02 0.02 0.02 0.01 0.03 0.04 0.07 0.03 0.03 0.06 0.03 0.02
0.37 0.48 0.29 0.40 0.64 0.67 0.54 0.54 0.56 0.69 0.42 0.54 0.65 0.56 0.51 0.52 0.54
6.8 5.9 7.4 6.8 4.9 4.5 5.5 5.5 5.4 4.2 6.3 5.1 4.5 5.2 5.4 5.5 5.5
8.9 11.2 8.0 9.4 8.3 12.2 11.3 10.7 10.8 14.7 8.1 11.3 13.4 12.7 16.0 13.6 12.8
2.8 3.0 2.4 2.6 2.4 3.1 2.8 2.9 3.1 3.3 2.8 3.1 3.3 3.0 3.3 3.2 3.1
0.92 0.94 0.91 0.94 0.86 0.95 0.91 0.92 0.97 0.95 0.93 0.95 0.96 0.94 0.95 0.95 0.96
0.53 0.58 0.77 0.83 0.51 0.70 0.46 0.52 0.62 0.57 0.67 0.60 0.60 0.52 0.56 0.60 0.62
Mean SD
18.8 2.1
271 178
33.6 9.8
0.45 0.11
0.03 0.02
0.52 0.11
5.6 0.8
11.4 2.3
2.9 0.3
0.93 0.03
0.60 0.09
Table 3 Summary of foraminiferal assemblage data and indices in all reef rubble samples assessed from Conch Reef, October 2008. (#Gen = number of genera, SB = symbiont-bearing taxa, ST = stress-tolerant taxa, Other = other smaller taxa, FI = FORAM Index, ˛ = Fisher Diversity, H = Shannon Diversity, D = Simpson’s Diversity Index, E = Evenness Index, SD = standard deviation). Site
Depth (m)
21 31 51 52 53 61 62 63 72 10 3 11 2 12 1 13 3 15 1 15 2 15 3 16 1 16 2 16 3 17 3 18 2
20 20 13 13 13 13 13 13 20 14 17 20 18 25 25 25 26 26 26 17 20
Mean SD
18.9 5.0
#/cm2 290 156 674 285 268 301 301 203 132 74 551 297 60 1116 534 1086 1059 1320 1094 644 198 507 390
# Gen
SB
ST
Other
FI
˛
H
D
E
47 48 45 45 49 49 49 49 50 48 54 55 45 43 51 50 54 53 57 54 42
0.23 0.25 0.17 0.17 0.18 0.17 0.19 0.22 0.22 0.20 0.13 0.18 0.25 0.22 0.21 0.20 0.24 0.22 0.16 0.18 0.39
0.03 0.06 0.06 0.07 0.08 0.05 0.06 0.10 0.10 0.05 0.13 0.11 0.06 0.06 0.04 0.06 0.05 0.07 0.07 0.05 0.02
0.74 0.69 0.77 0.76 0.74 0.79 0.75 0.69 0.68 0.75 0.73 0.71 0.69 0.71 0.75 0.75 0.71 0.72 0.78 0.77 0.59
3.8 3.9 3.3 3.3 3.4 3.3 3.4 3.6 3.6 3.6 2.9 3.3 3.9 3.7 3.6 3.5 3.9 3.7 3.2 3.4 5.1
8.2 12.9 12.3 13.3 15.0 12.1 11.7 13.0 12.7 13.7 13.5 13.1 12.5 11.5 14.7 13.0 15.2 13.5 13.1 12.3 13.8
3.3 3.2 3.2 3.3 3.2 3.2 3.1 3.1 3.1 3.2 3.1 3.1 3.1 3.2 2.4 2.7 2.6 2.5 3.2 2.0 2.7
0.95 0.95 0.95 0.95 0.95 0.95 0.93 0.94 0.95 0.95 0.95 0.96 0.95 0.95 0.93 0.96 0.95 0.95 0.95 0.93 0.91
0.64 0.67 0.64 0.68 0.63 0.61 0.57 0.63 0.73 0.68 0.64 0.54 0.72 0.71 0.27 0.33 0.31 0.30 0.57 0.16 0.57
49.4 4.0
0.21 0.05
0.07 0.03
0.73 0.04
3.6 0.4
12.9 1.4
3.0 0.3
0.94 0.01
0.55 0.17
abundant in sediments than in the rubble samples. Median S/R for smaller, more fragile taxa was 0.36, indicating that nearly twothirds of their shells were not represented in the sediment samples. In the sediment, representatives of four symbiont-bearing genera were recorded as alive when collected, based on color. In
the rubble, representatives of all nine common genera were found with symbiont color. Of the four taxa found live in both sample sets, Asterigerina and Peneroplis were found in similar percentages in both, while Laevipeneroplis was more than twice as likely to be found alive on rubble, and Amphistegina was 10
Table 4 Comparisons (t-statistic) of mean assemblage data and indices from sediment and rubble samples; means differ slightly from Tables 1 and 2 because data for sites where multiple samples were examined were combined so N = 13 and degrees of freedom = 12 for all t-tests. (#Genera = number of genera, SB = symbiont-bearing taxa, ST = stress-tolerant taxa, Other = other smaller taxa, FI = FORAM Index, ˛ = Fisher Diversity, H = Shannon Diversity, D = Simpson’s Diversity Index, E = Evenness Index, SD = standard deviation).
Sediment (mean) Sediment (SD) Rubble (mean) Rubble (SD) T-statistic Probability
# Genera
SB
ST
34.1 8.58 49.40 4.00 −7.06 1.3E−05
0.45 0.10 0.22 0.061 7.80 4.9E−06
0.026 0.012 0.068 0.031 −4.16 0.0013
Other 0.52 0.10 0.72 0.047 −6.15 5E−05
FI
˛
H
D
E
5.6 0.8 3.6 0.4 7.90 4.3E−06
11.4 2.12 12.9 1.41 −2.20 0.05
2.96 0.23 2.97 0.34 −0.23 0.83
0.94 0.02 0.94 0.01 −1.22 0.25
0.59 0.08 0.55 0.17 0.19 0.85
C.M. Stephenson et al. / Ecological Indicators 48 (2015) 1–7
Fig. 3. Cluster analysis (Bray–Curtis similarity) of square-root transformed, percentabundance data for foraminiferal assemblages from the sediment and rubble samples (#, # and #* indicate multiple samples from the same site).
times more likely to be collected live from rubble than from sand. 4. Discussion Foraminiferal assemblages of the Florida reef tract are well known (e.g., Bock, 1971; Culver and Buzas, 1982). Lidz and Rose (1989), working only with sediment samples from Florida, reported ∼50 foraminiferal species representing 32 genera and 20 families. Wright and Hay (1971) found 117 species representing 60 genera from the Florida reef tract. Both data sets included a wider range of environments than our data set from a single shelf-margin reef. The primary differences between our taxonomic list and previous studies were in recent generic distinctions, following Loeblich and Tappan (1987). Nevertheless, our results showed that the benthic foraminiferal assemblage on the Florida reef tract is well known, very diverse, and well represented even at a single reef location. Moreover, the genus accumulation curves revealed that a single
Table 5 Relative abundances of the 20 most common genera used to calculate a concentration ratio (S/R) for each genus. Genus
Sediment
Rubble
S/R
Amphistegina Archaias Articulina Asterigerina Bolivina Borelis Cibicides Cyclorbiculina Discorbis Gavelinopsis Laevipeneroplis Miliolinella Neoconorbina Planorbulina Pseudoschlumbergerina Pseudotriloculina Quinqueloculina Rosalina Siphonapteraa Textulariab
9.37 5.45 2.68 8.34 0.21 2.50 0.41 3.96 3.70 1.68 11.4 1.87 0.80 1.79 2.01 1.35 8.09 5.11 2.83 5.43
3.76 1.97 2.23 2.85 3.10 0.91 2.48 0.71 1.95 4.66 7.14 5.25 3.24 8.10 4.02 3.04 8.17 8.85 0.57 2.11
2.50 2.77 1.21 2.92 0.07 2.73 0.16 5.55 1.90 0.36 1.60 0.36 0.25 0.22 0.50 0.44 0.99 0.58 5.01 2.57
a b
Agglutinated miliolid. Agglutinated textularid.
5
sample is likely to recover at least half the common genera and that three samples are likely to recover about two-thirds of them. The samples overall were quite homogenous. The primary differences between sample types were in the relative abundances of smaller foraminifers. In both sample sets, more than 70% of the genera occurred at 1% abundance or less. The 12 genera not found in both sample types were uncommon, occurring in only one or two samples overall. Thus, the sediment assemblages, which were mostly dead shells, generally reflected the taxa living on the rubble/phytal substrates in the area, although not their proportions. More taxa were found in the rubble samples than in the sediment samples; smaller, more fragile taxa were clearly underrepresented in the sediments. Nevertheless, most of the sediment samples clustered with the rubble samples at greater than 60% similarity. This was actually somewhat surprising given the coarse texture of the sediments. Concentration ratios quantified the observation that the more robust taxa tend to be concentrated in the sediments compared to smaller and more delicate taxa. Amphistegina, Archaias, Asterigerina, Borelis, and Laevipeneroplis all exhibited ratios between approximately 1.5 and 3. Cyclorbiculina had the highest concentration ratio of the symbiont-bearing taxa; possibly an artifact of its larger, wingshaped structure, which may enhance transport of the shells from shallower environments (Hohenegger et al., 1999). Archaias, a similar symbiont-bearing Miliolida, has robust shells that are thick and reinforced by pillars, which allows the shells to be resistant to abrasion and winnowing and therefore to accumulate in carbonate sediments (Martin, 1986). The distributions of Asterigerina were notable. These foraminifers have intermediate-sized shells, are thick-walled, biconvex in shape, and host algal symbionts. The shells and even living specimens were found commonly in both sediment and rubble samples. Previous studies have noted the abundance of this species, and of the robust but smaller Discorbis rosea, in high-energy reef environments (Crevison et al., 2006; Ramirez, 2008; Baker et al., 2009). Besides D. rosea, two other smaller genera were found more than twice as commonly in sediment as on rubble. Siphonaptera, an agglutinated miliolid, was approximately five times more common, while Textularia, which belongs to the agglutinate Order Textularida, was about 2.5 times more common in sediment. Whether these differences indicate that the taxa live in sediments or are simply more resistant to destruction is not known, but one can speculate on both possibilities. In the first, sediment particles with which to build an agglutinated shell are more readily available to foraminifers living in the sediments. Siphonaptera was previously reported (Carnahan et al., 2009) to cluster with symbiont-bearing foraminifers that are indicative of oligotrophic environments. Two smaller miliolid genera, Articulina and Quinqueloculina, were found similarly represented in sediment and rubble samples (Table 5). Both genera are relatively diverse and some species in both genera have intermediate-sized, relatively thick shells. Again, members of these genera may be living in the sediment as commonly as on rubble, and those with relatively thick shells would have higher preservation potential (Boltovskoy and Wright, 1976; Wetmore, 1987). Previous studies comparing live and dead assemblages have commonly reported that living foraminifers are seldom abundant in sediment samples, and that diversities are higher in dead assemblages (e.g., Lynts, 1966; Scott and Medioli, 1980; Alve, 2000). Buzas et al. (2002) found that dead assemblages reflect the overall environment, while the live assemblage in any given sample may reveal a local bloom. Murray and Alve (2000) reported that substantial spatial variation can occur within a centimeter and that dead assemblages represent the time-averaged contribution of empty shells from the production of successive living assemblages, with
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C.M. Stephenson et al. / Ecological Indicators 48 (2015) 1–7
modification by postmortem processes. Studies comparing live and dead assemblages in reef-sediment samples (e.g., Cockey et al., 1996; Peebles et al., 1997) reported that foraminifers collected alive typically made up less than 10% of the foraminiferal shells identified. Our results reported here are consistent with such previous reports. Comparing live and dead assemblages was not a primary goal of our study as the samples we evaluated were not stained. Nevertheless, protoplasm color allowed symbiont-bearing taxa collected live to be easily distinguished from dead shells. The highest percentages of specimens collected live in sediments were 6% for Asterigerina and Laevipeneroplis. Amphistegina was about 10 times more likely to be found alive in the rubble samples than in the adjacent sediments. Similarly, Martin (1986) found Archaias living primarily on vegetation, with virtually no living Archaias in his sediment samples. We found neither Archaias nor Cyclorbiculina collected alive in sediment samples, though dead shells of both were common. Because these taxa have relatively large shells that are resistant to destruction, their dead shells are often abundant in the shelf sediments of the tropical western Atlantic and Caribbean (Martin, 1986; Triffleman et al., 1991; Peebles et al., 1997; many others). The FORAM Index (FI) was developed to reflect the response of the calcifying benthic community to the suitability of the environment for reef growth (Hallock et al., 2003). In our samples, the mean FI of sediment samples was 5.6 ± 0.8, indicating that the water quality at Conch Reef was suitable for accretion. The FI was developed using total assemblages from sediment samples because their collection adds minimal time to a field sampling effort. Moreover, collection of sediment samples for analysis of total assemblages does not require transport of preservatives, minimizing logistical considerations, as well as costs of collection and transport to the laboratory (Hallock et al., 2003). Some researchers have applied the FI to live reef assemblages (e.g., Barbosa et al., 2009; Koukousioura et al., 2011; Carilli and Walsh, 2012; Kelmo and Hallock, 2013), often yielding values in the 3–4 range. Our data set provided the opportunity to compare the FI values from rubble substrata, which more closely represented the live assemblage, and from the total assemblage from sediments. The mean FI for the rubble samples was lower, 3.6 ± 0.4; but still indicating a significant contribution by symbiont-bearing foraminifers, consistent with the assessment that water quality at Conch Reef supports calcifying symbioses. No significant differences were found between the means of other indices calculated (Shannon Diversity, Simpson’s Diversity, and Evenness) for sediment and rubble samples (Table 4); only FI, the number of genera per sample, and the Fisher ˛ exhibited differences. Hayek and Buzas (2010) recommended the use of the diversity and evenness indices for assessing assemblages, so the fact that those indices did not reveal significant differences between our rubble and sediment samples indicates the robustness of analyses based on total assemblages in reef environments. While taxonomic richness was higher in the rubble samples, when standardized to sample size using the Fisher ˛ index, the difference between the sediment and rubble samples was only marginally significant. In conclusion, the sediment reveals what taxa have been living in an area in the recent past and that are present at the time of sampling. The underlying observation for the FORAM Index is that sediments on healthy reefs have a larger proportion of shells of symbiont-bearing foraminifers compared to other smaller foraminifers and stress-tolerant foraminifers (Hallock, 1988; Hallock et al., 2003). Foraminifers found in the sediments are represented primarily by empty shells, while live specimens can be found living on a variety of substrates. According to Engle (2000, p. 3-1), “an ideal indicator of the response of benthic organisms to perturbations in the environment would not only quantify
their present condition in the ecosystems but would also integrate the effects of anthropogenic and natural stressors on the organisms over time”. “This information is precisely what foraminiferal shells in the sediments can provide” (Hallock et al., 2003, p. 223). Acknowledgments Field support was provided through NOAA contract number to NURC-UNCW: NA080AR4300863; subcontract to UNC-Chapel Hill: ARB-2008-11 (PIs: C. Martens and N. Lindquist); subcontract to USF: 5-46147 (PIs: P. Hallock Muller and R. Byrne). J. Scott Fulcher provided assistance in processing samples. Kendra Daly, Lisa Robbins, and anonymous reviewers provided comments that improved the manuscript. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.ecolind. 2014.07.004. These data include Google maps of the most important areas described in this article. References Alve, E., 2000. Environmental stratigraphy: a case study reconstructing bottom water oxygen conditions in Frierfjord, Norway, over the past five centuries. In: Martin, R.E. (Ed.), Environmental Micropaleontology. Kluwer Academic/Plenum Publishers, Boston, pp. 324–350. Baker, R.D., Hallock, P., Moses, E.F., Williams, D.E., Ramirez, A., 2009. Larger foraminifers of the Florida Reef Tract, USA: distribution patterns on reef-rubble habitats. J. Foraminifer. Res. 39, 267–277. Barbosa, C.F., Prazeres, M., de Freitas, Ferreira, B.P., Seoane, J.C.S., 2009. Foraminiferal assemblage and reef check census in coral reef health monitoring of East Brazilian margin. Mar. Micropaleontol. 73, 62–69. Bock, W.D., 1971. A handbook of benthic Foraminifera of Florida Bay and adjacent waters. In: Jones, J.I., Bock, W.D. (Eds.), A Symposium of Recent South Florida Foraminifera, vol. 1. Miami Geol. Soc. Mem., Miami, FL, pp. 1–72. Boltovskoy, E., Wright, R., 1976. Recent Foraminifera. Junk, The Hague. Buzas, M.A., Hayek, L.C., Reed, S.A., Jett, J.A., 2002. Foraminiferal densities over five years in the Indian River Lagoon, Florida: a model of pulsating patches. J. Foraminifer. Res. 32, 68–93. Carilli, J., Walsh, S., 2012. Benthic foraminiferal assemblages from Kiritimati (Christmas) Island indicate human-mediated nitrification has occurred over the scale of decades. Mar. Ecol. Prog. Ser. 456, 87–99. Carnahan, E.A., Hoare, A.M., Hallock, P., Lidz, B.H., Reich, C.D., 2009. Foraminiferal assemblages in Biscayne Bay, Florida USA: responses to urban and agricultural influence in a subtropical Estuary. Mar. Pollut. Bull. 59, 221–233. Clarke, K.R., Warwick, R.M., 2001. Changes in Marine Communities: An Approach to Statistical Analysis and Interpretations. PRIMER-E Ltd., Plymouth Marine Laboratory, UK, www.PRIMER-e.com Cockey, E., Hallock, P., Lidz, B.H., 1996. Decadal scale changes in benthic foraminiferal assemblages off Key Largo, Florida. Coral Reefs 15, 237–248. Crevison, H., Hallock, P., McRae, G., 2006. Sediment cores from the Florida Keys Reef Tract (USA): is resolution sufficient for environmental applications? JEMMM 3, 61–82. Culver, S.J., Buzas, M.A., 1982. Distribution of recent benthic Foraminifera in the Caribbean Region. Smithsonian Contrib. Mar. Sci. 14, 1–382. Cushman, J.A., Todd, R., Post, R., 1954. Recent Foraminifera of the Marshall Islands, Bikini and nearby atolls. 2. Oceanography (biology). U.S. Geol. Surv. Prof. Pap. 260-II, 319–384. Engle, V.D., 2000. Application of the indicator evaluation guidelines to an index of benthic condition for Gulf of Mexico estuaries. In: Jackson, L.E., Kurtz, J.C., Fisher, W.S. (Eds.), Evaluation Guidelines for Ecological Indicators. EPA/620/R-99/005, vol. 3. U.S. Environmental Protection Agency, Research Triangle Park, Durham, NC, pp. 1–29. Fabricius, K.E., Cooper, T.F., Humphrey, C., Uthicke, S., De’ath, G., Davidson, J., LeGrand, H., Thompson, A., Schaffelke, B., 2012. A bioindicator system for water quality on inshore coral reefs of the Great Barrier Reef. Mar. Pollut. Bull. 65 (SI), 320–332. Hallock, P., 1981. Algal symbiosis: a mathematical analysis. Mar. Biol. 62, 249–255. Hallock, P., 1988. The role of nutrient availability in bioerosion: consequences to carbonate buildup. Palaeogeogr. Palaeoclimatol. Palaeoecol. 63, 275–291. Hallock, P., 2012. The FORAM Index revisited: usefulness, challenges and limitations. In: Proceedings of the International Coral Reef Symposium, Cairns, Australia, 9–13 July 2012, http://www.icrs2012.com/proceedings/ manuscripts/ICRS2012 15F 2.pdf Hallock, P., Cottey, T.L., Forward, L.B., Halas, J., 1986. Population biology and sediment production of Archaias angulatus (Foraminiferida) in Largo Sound, Florida. J. Foraminifer. Res. 16, 1–8.
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