233

Hydrobiologia 144: 233-241 (1987) © Dr W. Junk Publishers, Dordrecht - Printed in the Netherlands

Impact of nutrient enrichment and alkalinization on periphyton communities in the New Jersey Pine Barrens Mark D. Morgan Department of Biology, Rutgers University, Camden, NJ 08102, US.A. Keywords: Pine Barrens, periphyton, pH, alkalinization, nutrients, disturbance

Abstract The impact of residential and agricultural development on stream periphyton communities in the New Jersey Pine Barrens was examined by comparison with communities in undeveloped areas. Watershed disturbance resulted in stream water primarily characterized by greatly elevated pH levels and nitrate concentrations. A total of 53 periphyton species were encountered in bimonthly samples over a one year period in the three disturbed and three undisturbed study streams. Species richness was significantly greater in the disturbed streams based on three criteria: the average number of species per stream on each sampling occasion (disturbed = 6.3; undisturbed = 4.9), the average number of species per stream for the entire year (disturbed = 19.3; undisturbed = 16.0), and the total number of species found in streams within a type (disturbed = 40; undisturbed = 31). Species composition also changed significantly as the result of disturbance. There appeared to be replacement of species characteristic of undisturbed Pine Barrens streams with species peripheral to the region. The expected effects of both elevated pH and nitrate were consistent with these results. Introduction Aquatic ecosystems are affected in many ways by human activities. The impact of nutrient enrichment and changing pH (mainly acidification) are well documented and have been shown to be particularly important in structuring aquatic algal communities (e.g., Schindler, 1977; Hall et al., 1980; Lazarek, 1982; Tilman, 1982). Although changes in these factors together have been only rarely examined, when studied separately, plant species diversity typically declines in response to increased nutrients and acidity (Hendrey, 1976; Harcombe, 1977; Axelrod et al., 1981; Schindler & Turner, 1982). The decline in species richness often results from the increased dominance of a few species at the expense of other members of the community. The Pine Barrens of New Jersey is a large (approximately 2 500 km2) mostly forested region that harbors many unique plant and animal communi-

ties (Forman, 1979). Since World War II, expansion of nearby urban centers has led to increasingly heavy agricultural and residential development of the area. A primary effect of this development on surface waters is nutrient enrichment and elevated pH (Pinelands Commission, 1980; Morgan, 1984). The purpose of this study was to determine how these factors together affect species richness and composition of periphyton in Pine Barrens streams. Study area The Pine Barrens occupies most of the southern half of New Jersey. The region is underlain by thick coastal plain sands which form droughty, nutrient poor, acidic soils (see Forman, 1979 for a comprehensive treatment). The upland vegetation is dominated by pitch pine (Pinus rigidaMill.) and a varie-

234 ty of oaks (Quercus spp.). The wetland communities occupy about 257o of the entire region and are dominated by pitch pine, Atlantic white cedar (Chamaecyparisthyoides L.) and red maple (Acer rubrum L.). Surface waters are fed primarily from groundwater discharge (Rhodehamel, 1979), and are typically nutrient poor, stained brown by humic materials and iron, and acidic (pH 3.5-4.5; Morgan, 1984). All study streams were located within the central portion of the Pine Barrens (Fig. 1). The headwater regions of the disturbed streams (Albertson Brook, Springers Brook, and Friendship Creek) were ex-

tensively developed for residential and/or agricultural uses. The undisturbed sites (Sleeper Branch, Skit Branch, and Burrs Mill Creek) were undeveloped, except for limited commercial cranberry or blueberry operations, which resulted in no significant nutrient enrichment. The sampling sites were carefully selected to be as comparable in hydrology and habitat as possible. All study sites were continuously flowing, second or third order streams, which drained similarly sized sub-basins (2000-9000 hectares). Disturbed and undisturbed streams were also paired within the same main drainage basin. In addition, sam-

Fig. 1. Map of the eastern United States showing a blow-up of the six sampling sites (large solid circles) within the central New Jersey Pine Barrens.

235 pling sites were chosen to yield a similar distribution of canopy (hardwood vs cedar, open vs closed) and habitat (backwaters, sand bars, bank slope) characteristics. Materials and methods Physical and chemical measurements were made on all streams approximately monthly from March 1982 through February 1983 within 48 hr of each other. The following parameters were measured: temperature, velocity, discharge, dissolved oxygen, conductivity, pH, alkalinity, nitrate, ammonia, total phosphorus, and total dissolved solids. See Morgan & Philipp (1986) for more detail on analytical techniques. Periphyton samples were collected bimonthly from three basic substrate habitats; submerged vegetation stems, submerged logs, and submerged backwater or bank detritus. All samples were preserved in 10% Formalin. Identification and enumeration of species were made by examining randomly chosen subsamples of all collections on wet mount slide preparations. Each slide was scanned using 100 magnification to determine general algal type and distribution. Identifications were made under 430 magnification. For samples with numerous diatoms that could not be identified from a wet mount slide, burn mount slides were prepared. An aliquot of sample was placed on the cover slip with distilled water and 30% H2 0 2 , and the liquid evaporated. The cover slips were then heated to 260°C for 15-20 min and mounted on slides using Hydrax medium. Major diatom types were identified using a 90x oil immersion objective. Algal identification was aided by use of the following references (Smith, 1933; Drouet & Dailey, 1956; Prescott, 1962; Patrick & Reimer, 1966, 1975; Drouet, 1968, 1978, 1981; Prescott et al., 1975, 1977; Hustedt, 1976; Ruzicka, 1977). Organisms that could not be identified to species were assigned to the same morphological form within a genus. A voucher specimen collection has been integrated with collections at the Philadelphia Academy of Natural Sciences, Philadelphia, Pennsylvania, U.S.A. Although relative abundance determinations are somewhat subjective due to varying growth forms, size of cells, and clumping of populations on the

slide, estimates were made using the following criteria: Dominant-predominant type throughout sample; Abundant-observed in most fields when examined under high dry magnification; Commonobserved in approximately 20% of sampled fields; Occasional-observed in less than 10% of sampled fields. To compare the relative abundances of species between stream types, numerical values of from 1 for occasional to 4 for dominant forms were assigned to the relative abundance data. These values were summed for all occurrences of a species within a stream type over time. This number was then divided by the total summed abundance value for both stream types to yield the percentage of the total abundance of a species accounted for by a particular stream type. Quantitative comparisons of species composition among streams was accomplished by use of Jaccard coefficients of similarity, such that J = a/(b + c) where a = the number of

species common to both streams, b = the total number of species in one stream, and c = the total number of species in the other stream (MuellerDombois & Ellenberg, 1974; Morgan & Philipp, 1986). Results A summary of the physical and chemical characteristics of the three disturbed and three undisturbed streams is presented in Table 1 (see Morgan & Philipp, 1986 for more detail). The large degree of variation apparent in many of these parameters reflected their seasonal nature. The impact of watershed disturbance on water quality was evident in three parameters; pH, alkalinity, and NO3-N. Average H+ concentration was an order of magnitude lower and NO3-N concentration an order of magnitude greater in the disturbed streams. Alkalinity was also elevated in the disturbed streams, but the actual values remained quite low. The disturbed streams, like their undisturbed counterparts, were characterized as extremely soft, poorly buffered waters. Consequently, the major characteristics distinguishing disturbed from undisturbed waters at these sites were elevated pH and NO3-N. Both pH values and NO3-N concentrations remained relatively constant throughout the year in

236 Table 1. Summary of the physical and chemical characteristics of the disturbed and undisturbed streams during the study. Values reported are the mean (range) for the 3 streams within each type. P is the significance level of an analysis of variance comparing the disturbed with the undisturbed streams. Parameter

Disturbed

Undisturbed

P

pH (units) Alkalinity (mgCaCO 3 1- ') NO--N (g 1-1) NH 3 -N (g 1-') Total P (g 1- l ) Conductivity (mhos) TDS (mg 1-') DO (% saturation) Temperature (C) Velocity (m s-') 3 Discharge (m s-')

6.8) 5.1 (4.2 5.3 (0 - 30) 425 (2 - 1385) (0 - 79) 25 17 (3 - 90) (32 - 254) 86 (33 - 123) 53 91 (64 - 103) 12 (1 - 24) 0.61) 0.31 (0.080.67 (0.022.56)

(3.6 - 4.9) 4.1 0.03 (0 - 0.1) 19 (0 - 45) 48 (0 -217) 12 (2 - 80) 71 (20 - 252) (5 - 125) 46 82 (52 - 108) 13 (0 - 26) 0.21 (0.03- 0.37) 0.35 (0.01- 2.33)

0.01 0.05 0.05 NS NS NS NS NS NS NS NS

general rareness of most species. For example, of all the restricted species, only five (Actinella punctata Lewis, Synedra ulna (Nitz.) Ehr., Tabellaria flocculosa (Roth) Kiitz, Eunotia exigua (Br6b ex. Kutz) Rabh., and Penium sp.) occurred more than twice out of a possible 18 times. The most frequently occurring species was Tabellariaflocculosa, which occurred six times. Other lines of evidence, however, suggest that major shifts in species composition did result from disturbance of these streams. For instance, ten of the species present in both stream types occurred fairly frequently (present in more than nine out of the possible 36 samples). The distribution of their relative abundance values within each stream type as a percentage of their total abundance is presented in Fig. 2. A Chi square (X2) test for random distribution of species abundances between stream types showed highly significant preference of some species for particular stream types (X2 = 59.17, 9 df, p < 0.001). In general, there appeared to be three distinct groups of species. The first group

the undisturbed streams (Table 2). These parameters, however, fluctuated dramatically in the disturbed streams. Comparisons of warm season season with cold (May-October) (November-April) data revealed that pH values were significantly higher (t = 2.24, n = 12, p < 0.05) and that nitrate concentrations were significantly lower (t=3.98, n = 12, p < 0.01) in the warm season. Periphyton occurrence by habitat type was extremely variable. Because the major objective of this study was to isolate the effect of watershed disturbance on the periphyton community structure, data on habitat type were pooled within a stream. A total of 53 periphyton species were encountered during this study (Table 3). A large number of species were restricted to one stream type or the other (Disturbed only= 22, Undisturbed only= 13). While the restricted nature of so many species was suggestive of a dramatic change in species composition associated with disturbance, such a conclusion from these data could be premature because of the

Table 2. Difference in pH and NO,--N in disturbed and undisturbed streams during cold (November-April) and warm (May - October) seasons. P = significance level based on t test. NS = Not Significant. Parameter

Stream Type

Warm

Cold pH (units) NO3--N (gl-

Disturbed Undisturbed l)

Disturbed Undisturbed

P

Season (Mean ± SE)

4.8 (4.7-4.9) 4.0 (4.0-4.1) 580 22

(72) (5)

5.6 (5.4-6.1) 4.2 (4.1-4.3) 269 16

(30) (4)

0.05 NS 0.01 NS

237 Table 3. List of attached algal species recorded during this study by stream type. For the disturbed and undisturbed only categories. An * indicates the species that have not been previously recorded from the Pine Barrens. Disturbed Only

Undisturbed Only

Actinella punctata Lewis

Both

Desmogonium rabenhorstianum var. elongatum Patr. *Eunotia exigua (Br6b ex. Kuitz) Rabh. E. flexulosa Br6b ex. Kiitz *E. tautoniensis Hust. ex. Patr. Eunotia sp. *Frustuliarhomboides

Bulbochaete sp. Calothrix sp. *Chaetophorasp. *Closterium kuetzingii Br6b C. ralfsii Br6b ex. Ralfs

Asterionellaformosa Hass. Audouinella violacea (Kutz) Hamel Batrachospermum sp. Closterium sp. Cosmarium sp. Eunotia curvata (Kutz) Lagerst.

var. saxonica (Rabh.) Det.

Micrasteriasrotata (Grev.) Ralfs

*Frustuliarhomboides var. capitata (A. Mager) Patr.

Micrasteriassp. Penium sp. *Pinnulariasocialis (T. C. Palm) Hust. P. substomatophoraHust. P. viridis (Nitz) Ehr. *Schizothrix calcicola (Ag.) Gom.

*F. vulgaris (Thwaites) Det. Gomphonema parvulum Kutz Nitzschia obtusa W. Sm. Nitzschia sp. Pinnulariagibba Ehr. Pleurotaenium sp. *Porphyrosiphonsplendicus (Grev.) Dr. *Radiofilum sp. Schizothrix mexicana Gom. · Schizothrix sp. *Staurastrumsp.

E. incisa W. Sm. ex. Greg. E. pectinalis (O. F. Mull) Rabh. E. serra Ehr. Frustuliarhomboides (Ehr.) DeToni Microspora sp. Mougeotia sp. *Schizothrixfriesii (Ag.) Gom. Spirogyra sp. Tabellariafenestrata (Lyrgb.) Kiitz Tetraspora sp. Zygnema sp. Zygogonium ericetorum Kiitz

Synedra ulna (Nitz.) Ehr.

Tabellariaflocculosa (Roth) Kutz Ulothrix sp. *Vaucheria

sp.

consisted of four species that were clearly more abundant in undisturbed habitats (Batrachospermum sp., Frustulia rhomboides (Ehr.) DeToni, Spirogyra sp., and Zygogonium ericetorum Kutz). I

I _

100-

Undleturbd DIaturbod

a 8

60

0

III

Ba

Fr

89

I Zy

CI

n Eu

I 1111

MU

Au

MI

Ta

Species

Fig. 2. Relative abundance of periphyton species found in both disturbed and undisturbed streams. See Methods for detail on how relative abundance values were calculated. Key to species: Ba = Batrachospermum sp.; Fr = Frustuliarhomboides; Sp = Spirogyra sp.; Zy = Zygogonium ericetorum; C1 = Closteri-

um sp.; Eu = Eunotia pectinalis; Mo = Mougeotia sp.; Au = Audouinella violacea; Mi = Microspora sp.; Ta = Tabellaria fenestrata.

The second group consisted of species clearly more abundant in the disturbed streams (Closterium sp., Eunotia pectinalis (0. F. Mill) Rabh., Mougeotia sp.), and the third group showed no apparent preference (Audouinella violacea (Kiitz) Hamel, Microspora sp., Tabellaria fenestrata (Lyngb.) Kitz). Another line of evidence suggesting that disturbance resulted in a change in species composition comes from the distribution of newly reported genera and species for the Pine Barrens. Most species listed in Table 3 have been previously reported from the Pine Barrens (Moul & Buell, 1979, Patrick et al., 1979). However, five new genera and 15 new species are listed in the Table. Four out of the five new genera and nine out of the 15 new species occurred only in the disturbed streams. This heavy representation of new species and especially new genera in the disturbed streams suggests that disturbance may have opened these streams to colonization by species peripheral or non-indigenous to the Pine Barrens, thus resulting in a major change in species composition.

238 Table 4. Percentage community similarities (Jaccard coefficients) for comparisions within and between stream types. Individual comparisons are based on species composition data for each stream on each sampling date. Pooled comparisions are based on pooled species composition data for a particular stream over all sampling times. t is the student-t value and P is the level of significance. o Similarities

Individual comparisons comparisions

comparisions

t

P

turbed: x = 6.3, n = 18; undisturbed: X = 4.9, n = 18; t = 2.06; p < 0.05). A similar relationship

within types

between types

15.8 10.2 36

11.4 10.0 54

2.00

0.05

Pooled 27.6 SD 6.9 n 6 n 6

21.5 3.3 9 9

2.24

0.05

SD n

cies composition even among matched streams. Thus, factors unrelated to disturbance and not measured in this study must also play a major role in determining periphyton species composition at a particular location in a particular stream. Average species richness (number of species per stream) was significantly greater in the disturbed streams based on each sampling occasion (dis-

Differences in species composition between disturbed and undisturbed periphyton communities were examined quantitatively by use of Jaccard coefficients of similarity. Similarities ranged from a low of 0, meaning that there was no overlap in species between the two streams, to a high of 37%o. J = 100% would represent complete overlap in species composition. Based on individual comparisons for each sampling period, similarity values for comparisons within stream types were significantly greater than for comparisons between stream types (Table 4). In other words, periphyton communities within a stream type were significantly more similar to each other than to communities from the other stream type. If the data are pooled over all sampling periods for each stream, the same trend held, though the calculated similarities increased by about 10%. The overall low values of the similarity coefficients for all comparisons, however, suggest that there is much heterogeneity in periphyton spe-

was evident for the average number of species per stream pooled over the sampling period (disturbed = 19.3; undisturbed = 16.0), and for the total number of species found in all disturbed and undisturbed streams (40 vs. 31, respectively). Despite these differences in species richness, disturbance had no significant effect on the proportion of species found among the different taxonomic groups (Table 5). The hypothesis of independent assortment of species within taxonomic groups by stream type based on a Chi square (x2) test was accepted for all species (X2 = 2.15) and for the restricted species considered separately (X2 = 4.30). However, though not significant, diatoms appeared to be under represented and greens over represented in the disturbed streams, especially among the restricted species. Discussion The findings of this study closely parallel those of two recent studies on the effect of agricultural and residential development on Pine Barrens stream macrophyte and swamp communities (Ehrenfeld, 1983; Morgan & Philipp, 1986). In all three studies, the primary response of the aquatic community to disturbance was an increase in spe-

Table 5. Distribution of species between stream types by taxonomic unit. Restricted species are those found only in one stream type or the other. Taxon

Cyanophyta Chlorophyta Bacillariophyta Rhodophyta

All Species

Restricted Species

Disturbed

Undisturbed

Disturbed

Undisturbed

5 17 16 2

2 10 17 2

4 9 9 0

1 3 9 0

239 cies richness compared with natural Pine Barrens communities. In addition, Ehrenfeld (1983) and Morgan & Philipp (1986) reported that disturbance led to large scale replacement of species typical of the Pine Barrens with marginal or non-indigenous species. Historically, the natural Pine Barrens periphyton communities are poorly known, and for what is known, collection habitats have been rarely characterized in terms of disturbance. Thus, distribution data alone can be misleading as far as identifying a native flora. For instance, both Moul & Buell (1979) and Patrick et al. (1979) classified Tabellaria flocculosa as being particularly characteristic of the Pine Barrens based on distributional data. Yet, data from this study strongly suggest that this species is highly favored only under disturbed conditions (Table 3). Thus, it is not possible at this time to identify a characteristic periphyton flora to determine if disturbance resulted in significant species replacement. However, the large number of species found only in disturbed or undisturbed streams, and the high proportion of newly reported genera and species restricted to disturbed streams suggests that species replacement did result from watershed disturbance. A similar conclusion is evident from the abundance data for species found in both stream types (Fig. 2). There was a clear distinction between those species which seemed to benefit from disturbance and those which appeared harmed. Several recent studies have looked at the effect of changing pH (usually via acidification) on lake and stream periphyton communities. In general, periphyton species richness declines as aquatic environments become more acidic (Hendry, 1976; Hall et al., 1980; Miiller, 1980; Schindler & Turner, 1982). In the Pine Barrens, the naturally acidic stream water became less acidic as a result of disturbance, and periphyton species richness significantly increased. If one assumes that the effect of increasing pH in naturally acidic water is the reverse of acidifying near neutral water, then the Pine Barrens results are consistent with these previous reports. Detailed analysis of the community similarity data and seasonal pH trends suggests that pH changes alone, however, cannot account for all of the periphyton changes. For instance, the pH of disturbed and undisturbed streams converged in the

winter, while NO3 concentrations significantly diverged (Table 2). If pH were the primary factor affecting periphyton species composition, the between stream similarity coefficients for the winter months (November, January, March) should be greater than for the summer months (May, July, September). In fact, the opposite was true. Mean similarity coefficients for individual comparisons between stream types were greater in summer (J = 13.3%, n = 27) than in winter (J = 9.7%, n = 27), so periphyton species composition in dis-

turbed and undisturbed streams was less similar in winter. Similarity coefficients within stream types were not affected by season (winter = 15.4%, n = 18; summer

= 16%, n = 18). Thus, the sig-

nificantly elevated nitrate concentrations also appear to have contributed to the effect of disturbance on periphyton. The major effect of nutrient enrichment on terrestrial and aquatic plant communities is generally a decrease in overall species richness, as some species come to dominate the community (e.g., Lawes & Gilbert, 1880; Willis, 1963; Thurston, 1969; Schindler, 1977). Rarely do new species invade and replace existing species. These expected effects of enrichment contrast sharply with the increased species richness and altered species composition that resulted from nitrate enrichment of the Pine Barrens periphyton community. This apparent contradiction has been noted elsewhere for Pine Barrens swamp and stream macrophyte communities (Ehrenfeld, 1983; Morgan & Philipp, 1986). The possible explanations for these differences involve both the scale of the affected areas and the actual magnitude of the enrichment. As pointed out by Ehrenfeld (1983) enrichment studies often look for effects of elevated nutrients based on small plots or microcosms within a larger undisturbed habitat. In such a situation, the potential number of species capable of responding is greatly limited by the difficulty of immigrating to the test areas. In the Pine Barrens, enrichment is a regionwide phenomenon and peripheral species have an abundant opportunity to invade and colonize disturbed habitats. In fact, most of the species that replaced Pine Barrens species in the swamp and stream macrophyte communities were common peripheral species. Further evidence suggesting that increased species richness and altered species composition could

240 result from elevated nutrients comes from theoretical studies on the effect of enrichment in very nutrient poor systems (Tilman, 1982). Tilman argued that if total enrichment was low, an initial increase in species richness was expected followed by decreased species richness as enrichment continued. In the Pine Barrens, undisturbed streams exhibited very low concentrations of both N and P (Table 1) and based on N:P ratios appeared to be N limited (Morgan & Philipp, 1986). Disturbance greatly increased N but P remained very low. Thus, the disturbed streams apparently quickly switched from N to P limitation with the overall level of enrichment being relatively small. The resulting increase in periphyton species richness is then consistent with Tilman's theoretical conclusions.

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