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Stream biodiversity: The ghost of land use past J. S. Harding, E. F. Benfield, P. V. Bolstad, G. S. Helfman, and E. B. D.

Jones, III PNAS 1998;95;14843-14847 doi:10.1073/pnas.95.25.14843 This information is current as of December 2006.
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Plecoptera. Natl. In contrast. e-mail: jon@ environment. P. and lake ecosystems (1–4). the degree to which biological communities can recover from long-term disturbance is still relatively unknown. In many regions. VA 24061. (iv) land use within a 30-m riparian zone of the stream (up to 1 km upstream of the sampling site). Nelson. December 1998 Ecology Stream biodiversity: The ghost of land use past J. Our findings indicate that past land-use activity. and water chemistry. Sci. aerial photographs. V. and a qualitative sample was taken from a range of microhabitats within the reach. This paper was submitted directly (Track II) to the Proceedings office. marine. Considerable emphasis has been placed on protection or revegetation of riparian zones as a tactic for preserving aquatic ecosystems (16. and continental scales has received increasing attention as human disturbance and modification of ecosystems increase. AND E. Conservation of species diversity at local. resource-extraction projects. and reduce sedimentation in disturbed watersheds (18–20). HELFMAN¶. and maintenance of such biodiversity may require conservation of much or all of the watershed. Conditions in the riparian zone. substrate characteristics. JONES IIIʈ *Department of Biology. by attention only to land adjacent to the stream. S.S. © 1998 by The National Academy of Sciences 0027-8424͞98 ͞9514843-5$2. by emphasizing restoration of riparian zones. and approved September 24. and how long does recovery take? Although recovery and restoration of the physical habitat is often possible. †Present address: Cawthron Institute. strongly influence stream hydrology.cawthron. The seven spatial scales selected included both different riparian widths and longitudinal distances along the stream continuum as follows: (i) land use over the entire watershed. Stream ecologists have long recognized the strong dependence of streams on the surrounding terrestrial environment (12–15).C. Woods Hole Research Center. many rivers and streams have been profoundly modified by urban and agricultural development. impoundment. USA Vol. 11). Paul. 22). University of Georgia.Proc. 17). However. Private Bag 2. St. 23). and Trichoptera taxa. ¶Institute of Ecology. the Little Tennessee and the French Broad 6 were currently primarily forested and 6 were agricultural. MN 55108-1027. (vi) land use within a 100-m riparian zone of the stream (up to 1 km upstream of the sampling site). (v) land use within a 30-m riparian zone of the stream (up to 2 km upstream of the sampling site). ‡To whom reprint requests should be addressed. B. Atlanta. GA 30346-1278 Edited by George M. E. Fish were sampled by electroshocking and seining a 50-m reach. Land use in these 24 watersheds was assessed by determining the percentage of the watershed in forest at seven spatial scales for the 1950s and 1990s and was calculated from Geographic Information System overlays constructed from topographic maps. We used two approaches in the 14843 . D. Blacksburg. ref. Fish samples were taken at each site during spring and fall of 1995 and 1996. GA 30602. G. This process of reforestation allows us to ask: to what extent are the effects of human disturbance reversible. reforestation of previously cleared watersheds is occurring as agriculture becomes less important to the local economy (10. number of Ephemeroptera. 14843–14847. A modified quantitative kick net (0. This assumption is not supported by recent studies (21. whereas riparian land use and watershed land use in the 1990s were comparatively poor indicators. Woodwell. water quality. To achieve these aims. Athens. Abbreviations: DCA. Comparisons of diversity and land-use data were made with multiple regression models. in western North Carolina. F. Worldwide. and stepwise regression analysis was used to identify the combination of history and spatial land use acquired from the Geographic Information System that best explained the diversity of stream invertebrates and fishes. and pollution. land managers assume that stream conditions across the whole catchment can be mitigated The publication costs of this article were defrayed in part by page charge payment. (iii) land use within a 100-m riparian zone of the stream (for the entire length of the stream). empirical evidence of extirpations and extinctions of invertebrate species in lotic (running water) ecosystems is comparatively sparse (1–9).750 to 40. 1998) ABSTRACT The inf luence of past land use on the presentday diversity of stream invertebrates and fish was investigated by comparing watersheds with different land-use history. The riparian zone bordering streams serves as a buffer between the stream and the surrounding watershed and is also the primary source of organic matter for many small streams in forested biomes (12–15). which in turn affect all trophic levels. 250-␮m mesh) was used to collect five samples. Woods Hole. §Department of Forest Resources. Acad. Whole watershed land use in the 1950s was the best predictor of present-day diversity. The first was to compare diversity in streams that drain agricultural land to diversity in streams that drain forested land.00 ͞0 PNAS is available online at www. Invertebrate assemblages for each of the 24 streams were also compared by detrended correspondence analysis (DCA. The presence of natural vegetation in riparian zones has been shown to improve stream hydrology. and (vii) land use within a 100-m riparian zone of the stream (up to 2 km upstream of the sampling site). BENFIELD*. we investigated 24 tributary watersheds ranging from 1.4 m2. detrended correspondence analysis. regardless of reforestation of riparian zones.pnas. 115 Perimeter Center Place. S. EPT. pp. New Zealand. University of Minnesota. temperature regimes. Of the 12 watersheds chosen within each basin. MA. therefore. such as the southern Appalachian Mountains. particularly agriculture. The second was to examine the land-use history associated with the streams to look for clues that might help explain present-day diversity patterns. may result in long-term modifications to and reductions in aquatic diversity.700 ha in size in two river basins. HARDING*†‡. and satellite imagery from the 1950s and 1990s. The overall objective of the present study was to investigate relationships between land use and invertebrate and fish diversity in streams. BOLSTAD§. (ii) land use within a 30-m riparian zone of the stream (for the entire length of the stream). At each of the 24 streams. Virginia Polytechnic Institute and State University. and ʈCH2M Hill. Our understanding of the magnitude of species decline is clearest for vertebrates in terrestrial. §1734 solely to indicate this fact. 1998 (received for review May 4. regional. channelization. including a riffle-pool complex. Preservation of habitat fragments may not be sufficient to maintain natural diversity in streams. random benthic invertebrate samples were collected in 1995–1996 from riffles along a 10-m reach. This article must therefore be hereby marked ‘‘advertisement’’ in accordance with 18 U.

and total abundance were significantly greater in agricultural streams than in forested ones (Table 1). unpublished data). Paul and J. 2). Furthermore. Invertebrate taxonomic richness and other analogs of diversity [Margalef’s Index and the number of Ephemeroptera. personal communication). Meyer. A stepwise regression of DCA Axis 1 values was carried out against the 14 time and space Geographic Information System values for percentage of each watershed in forest (r2 ϭ 0. and for these streams and the French Broad agricultural streams it was 0. Both of these streams drain watersheds that were 92% forested in the 1990s. when analyzed separately. and Ͻ1% were native brook trout). significant differences in both faunal diversity and assemblage composition were observed between agricultural and forested streams. which experienced greater agricultural development in the past. but they were abundant at the other French Broad forested streams. the two forested streams were embedded in a landscape with high percentages of riparian agriculture (43% and 44%). Ͼ99% of trout were introduced rainbow and brown trout. generally showed stronger links to the past than agricultural watersheds in the Little Tennessee Basin. Reforestation of the riparian zone over the last 47 years has resulted in little effective recovery of the fauna of these Streams in 1990s forested watersheds were generally Ͼ90% forested in the 1950s. In contrast. These findings support our assertion that in currently forested watersheds. historic land-use data may be more useful indicators than present land use in predicting taxonomic diversity.14844 Ecology: Harding et al. the strongest predictor was land use in the 1990s in the 100-m riparian zone. In both river basins. F ϭ 28. 1950s watershed conditions best explained combined fish and invertebrate diversity across all watersheds. and sedimentation seemed to be linked to a reduced abundance of fishes belonging to the crevice-spawning reproductive guild (G. Therefore when considered separately. the North Carolina Biotic Index. but the invertebrate assemblages more closely resemble those of agricultural streams (Fig. Sculpin and trout were absent at both of these streams and were essentially absent from five of six agricultural streams. 1). These two streams were also anomalous with respect to fish species composition. The mean Jaccard similarity coefficient between these two anomalous streams and the other French Broad forested streams was 0. Plecoptera. Finally. Of these 12 species. The best predictor of invertebrate composition in these two forested streams was land use in the 1950s in the 30-m riparian zone up to 2 km upstream of the sampling site. Sci. The two means were significantly different (t test. and Trichoptera taxa (EPT)] were significantly greater in forested streams than in agricultural streams in both river basins (Table 1). Multivariate analysis incorporating invertebrate assemblage data for all streams shows that forested and agricultural streams differ in taxonomic composition.56.001). Fish diversity was greater where trout were absent and where species tolerant of sedimentation were favored. Land-use conditions in the 1950s in the 30-m riparian zone were the best predictors of invertebrate diversity. invertebrate density did not differ significantly between current land-use types.32.H.S. indicating that these forested streams were more similar to agricultural than to other forested streams. diversity (Margalef’s index). We found a significant negative correlation between fish-species diversity and trout abundance (n ϭ 24 streams.001). Margalef’s index. 5 occurred at no other forested stream. Natl. whereas those in the French Broad Basin averaged Ϸ30% forest (Fig. streams in 1990s agricultural watersheds in the Little Tennessee Basin averaged Ϸ60% forest in the 1950s. 12 of which they held in common. P Ͻ 0. the best single model for explaining invertebrate taxonomic richness was land use across the entire watershed in the 1950s (Table 2). Each column represents six watersheds characterized by 1990s land use in the basins of the Little Tennessee and the French Broad Rivers (data assessed from the Geographic Information System). and EPT values (which account for disturbance-sensitive taxa) in combined basins (Table 2). However. within 1 km upstream of the sampling sites (Table 2). land use in the historically more developed French Broad Basin showed consistently stronger regression values than in the Little Tennessee Basin. These forested sites contained 15 and 14 fish species. P Ͻ 0.. Again. Legacies of land use also help to explain the current composition of invertebrate assemblages in the study streams. . the French Broad Basin. and abundance in both the combined basins and in the Little Tennessee were 1950s land use at various spatial scales. with the exception of two forested streams (Fig. 1. Proc.16. FIG. In the 1950s. whereas 4 of these 5 were recorded in at least one agricultural stream. When data from both basins were combined. Substrate analysis of percentage of fine sediments indicated greater quantities in agricultural than forested streams (M. the total number of fish species. P Ͻ 0.42. as measured by Margalef’s Index. Invertebrate density was only weakly correlated with land-use patterns. USA 95 (1998) Regressions of diversity and watershed conditions across time and space showed that land use in the 1950s was usually the best indicator of present-day diversity.001. Percentage of watershed (within a 30-m riparian zone) in different land uses in the 1950s and 1990s. having assemblages more similar to the agricultural streams than other forested streams. The best single variable models for fish species richness. Acad. Fish assemblages showed a different trend. However. 2). our findings indicate that large-scale and long-term agricultural disturbances in a watershed limit the recovery of stream diversity for many decades. df ϭ 78. species richness and diversity in the French Broad basin alone were best explained by more localized land-use data in the 1990s (Table 2).

‫ءء‬ ‫ء‬ ‫ءء‬ n. we found that fishes dependent on the streambed for foraging or breeding (e. 2k.34 28.01 4. agriculture combined) and river basin (all Little Tennessee vs.4 3.7 Ϯ 0.69 0.82 0.2 Mean diversities are given ϮSE ( n ϭ 6).9 6.7 Ϯ 0.3 4. P Ͻ 0.04 6.3 4.2 22. Broad) 39.8 Ϯ 2.70 2. 1k. Tennessee) 48.46 0. Proc. land use over the entire watershed. Current stream restoration philosophy and policy supports the idea that recovery of stream fauna can occur relatively rapidly after short-term natural and human disturbances when riparian conditions are returned to a predisturbance state (24–26).7 Ϯ 1858 3.02 0.2 Agriculture (Fr.Ecology: Harding et al.3 4. and darters) were replaced in agricultural streams by species that dwell in the water column or those that clean sediment from their nests (e.s..37 0.1 Ϯ 45.94 3.69 0. land use within a 30-m riparian buffer zone of the stream. sediment-free streambed (27–29).17 9.3 Ϯ 7.s.53 0.6 4.37 22.46 0.8 5. n.s. sculpins.45 0.2 Ϯ 32.) †North Carolina Biotic Index . NCBI.30 19. Margalef’s index EPT NCBI† Invertebrate density Fishes Species richness Margalef’s index Fish abundance Total fish ϩ invertebrate taxa Combined river basins analysis consists of data for 24 watersheds.36 0.8 Ϯ 3.46 0.1 Forest (Fr.s. n.7 9.9 22. Our findings challenge assumptions about both the maintenance and future recovery of biodiversity in disturbed stream Table 2.25 12. River basin F 0. whereas French Broad and Little Tennessee River data are for 12 watersheds in their respective basins.86 2. 100.48 P n.1 Agriculture (L.53 0. n.06 0.0 Ϯ 3.5 Ϯ 3.40 0.0 Ϯ 5.7 Ϯ 6. Acad.4 0.g.4 3. 30.5 Ϯ 2.77 11. (‫ ء‬.56 4. (WS. ‫ءء‬ ‫ء‬ ‫ءء‬ ‫ءء‬ n.4 0. The difference in response between invertebrate and fish diversity may be caused by a stronger dependence of invertebrates (especially EPT taxa) on the presence of a relatively stable.67 0. ‫ءء‬ ‫ءء‬ ‫ءء‬ ‫ءء‬ ‫ءء‬ n.23 0.51 0. land use up to 1 km upstream from the sampling reach.73 0.05.4 Ϯ 3015 5.4 Ϯ 0.32 0.23 22.67 0. Table 1.3 27.01. n.5 757 Ϯ 149 71. USA 95 (1998) 14845 Mean diversity for forested and agricultural streams in the Little Tennessee and French Broad Rivers Forest (L.03 31.75 P ‫ءء‬ ‫ءء‬ n.2 Land use F 8.7 0.3 Ϯ 7.86 9.4 2212 Ϯ 354 71. Our data suggest that recovery requires decades.88 20.88 6. Sci.g.s. Results of two-way ANOVA are shown.2 Ϯ 2.73 0.14 1.33 8.22 6.s. ** P Ͻ 0.s. n.28 0.s.22 0. As well as differences in overall fish diversity.4 0. French Broad) treatments. not significant.6 0.6 0.9 Ϯ 40.9 0.3 16. Diversity indices Invertebrates Taxonomic richness Margalef’s index EPT NCBI† Invertebrate density Fishes Species richness Margalef’s index Fish abundance Fish ϩ invertebrate Species richness Ϯ 496 Ϯ 211 Ϯ 758 Ϯ 1958 14.s.4 6. Natl.27 0.2 Ϯ 25.) streams to predisturbance conditions.. Broad) 59. with Tukey’s test for land use (all forest vs.40 0.0 Ϯ 3.08 11.s.3 11.2 Ϯ 7.47 0.5 Ϯ 1441 7.76 2. land use within a 100-m riparian buffer zone of the stream.56 0.s.33 12.79 8.6 1772 Ϯ 377 56. not significant. Multiple regression analyses of measures of diversity against percentage of the watershed in forest at 14 different spatial scales and at two time periods Basins Invertebrates Taxonomic richness Combined river basins French Broad River Little Tennessee River Combined river basins French Broad River Little Tennessee River Combined river basins French Broad River Little Tennessee River Combined river basins French Broad River Little Tennessee River Combined river basins French Broad River Little Tennessee River Combined river basins French Broad River Little Tennessee River Combined river basins French Broad River Little Tennessee River Combined river basins French Broad River Little Tennessee River Combined river basins French Broad River Little Tennessee River Time and spatial watershed scales 1950-WS 1950-WS 1950-1k-30 1950-WS-30 1950-WS 1950-1k-100 1950-WS-30 1950-WS 1950-WS 1950-WS-30 1950-WS-100 1990-1k-100 1990-1k-100 1990-1k-30 1990-1k-100 1950-2k-30 1990-1k-100 1950-WS 1950-2k-30 1990-1k-100 1950-WS 1950-1k-100 1950-2k-100 1950-2k-100 1950-WS 1950-WS 1990-WS-30 r2 0. North Carolina Biotic Index.s.7 Ϯ 8.3 Ϯ 2635 3.8 Ϯ 4.2 Ϯ 1.59 0. ‫ ءء‬.09 4.9 1096 Ϯ 256 73. *P Ͻ 0.s.87 12. Only best single variable models are shown.01. Tennessee) 59. P Ͻ 0.25 0.9 21.s.07 F 27. some minnows.56 0.. ‫ء‬ ‫ءء‬ ‫ء‬ ‫ءء‬ ‫ءء‬ ‫ءء‬ n. other minnows and sunfishes).7 Ϯ 0.2 23.51 0. land use up to 2 km upstream from the sampling reach.s. n. n. n.04 1.s. ‫ء‬ n.. ‫ءء‬ ‫ءء‬ ‫ء‬ ‫ء‬ ‫ء‬ n.7 3.s.21 P ‫ءء‬ ‫ءء‬ ‫ءء‬ ‫ءء‬ n.4 12.82 18.7 Ϯ 1.2 6.4 0.05.

M. K. B. Williams. Martin. Johnson. M. floods. B.g.. ContrerasBalderas. Meyer. Exploitation and development of natural watersheds is continuing worldwide. M. London).. McAllister. & Burr. biotic communities. ecosystems. however. Jr. which is often unrecorded or unknown. E. the influence of forestfragment size on biodiversity has been investigated intensively (38). (1989) Fisheries 14. and point-source pollution) have often shown relatively rapid recovery of biotic communities (30–35). Our findings provide new insights into possible causes of variability in the diversity and composition of aquatic assemblages. 4. H. 2–20. construction.14846 Ecology: Harding et al.. Natl. A. In contrast. W. forested and agricultural streams (as indicated by the ellipses). D. 426. Proc. and these findings have provided the cornerstone of accepted theory and policy. Streams are grouped into two general clusters. 37). J. D. Studies of the recovery of stream assemblages after short-term catastrophic disturbances (e. Schindler. 2. H. Acad. E. our results support the view that conservation of natural ecosystems may require preservation of the entire watershed—not just fragments of it as many current policies assume. 6. E. Our results suggest that some of this variability may be a legacy of land use. MA). Groombridge. R. M. M. 1. R. World Conservation Monitoring Centre (1992) Global Biodiversity: Status of the Earth’s Living Resources. such as sustained agriculture. This research was supported by National Science Foundation Division of Environmental Biology Grants 9011661 and 9416803. Sci. Current land-management practices often operate on the assumption that economic activity within a catchment can proceed as long as riparian zones are preserved (36.. Warren.. J. our results indicate that the amount of forest and possibly forest size may be critical in influencing stream biota. Allan. J. and J. Webster for constructive comments. L. H. J. P. We suggest that disturbance of these systems. Few studies have assessed recovery from prolonged disturbance or scrutinized changes from a multiple-watershed perspective. (Chapman & Hall. D.. and watershed conditions is far from complete. Cambridge. Scott provided assistance with data collection and analysis. D. (1989) Bioscience 39. and the effects of this disturbance may be persistent. may result in substantial long-term modifications and reductions in natural biodiversity. Realization of the potential alteration or loss of biodiversity from watershedwide land use should provide a warning for conservation organizations and policy makers alike. which in our study involved the conversion of forest to agriculture.. USA 95 (1998) FIG. 6–18. Wilson. (1994) Fisheries 19. Paul. S. E. J. M. A. S. In terrestrial systems. L. J. & Deacon. 2. Bennett. & Flecker. We thank B. However. Navarro-Mendoza. ed. this issue has been largely ignored in stream systems. 3. logging.. Two outlier forested streams within the agricultural cluster represent streams that today lie in forested watersheds but were in partially agricultural watersheds in the 1950s. E. McTammany. Pulliam. and M. DCA of invertebrate assemblages based on presence͞absence data for the 24 watersheds in two river basins. but our understanding of the linkages among ecological processes that shape biodiversity. (1993) Bioscience 43. J. J. . 32–43. Finally. Jones. Neatrour. 5. Riparian zones have been used effectively to mitigate the adverse effects of many land-use practices. In addition to understanding the value of intact riparian zones. Data from studies of multiple streams are often highly variable and difficult to interpret. J. Wagner. L. may profoundly alter biotic communities. experimental manipulation. Harper. our study provides evidence of the importance of past land use as a determinant of present species diversity in streams. O. Simon. R. L. high impact or sustained anthropogenic disturbance. Press. Williams. Hendrickson. Pape. (1992) The Diversity of Life (Harvard Univ. Tank. D..

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