Report

Sarah J. Davies, Sarah E. Metcalfe, Fernando Bernal-Brooks, Arturo Chacon-Torres, John G. Farmer, A. B. MacKenzie and Anthony J. Newton

Lake Sediments Record Sensitivity of Two Hydrologically Closed Upland Lakes in Mexico to Human Impact
We provide evidence of rapid, recent environmental change in two lakes in the highlands of central Mexico. Multiple sediment cores were obtained from Lago de Zirahuen (Michoacan) and Laguna de Juanacatlan (Jalisco). Analysis of diatom assemblages, magnetic susceptibility, and metal concentrations was carried out, with the chronology provided by 210Pb dating, 14C dating, and tephrochronology. There is evidence of catchment disturbance during the colonial period in both basins, but the most striking feature at both sites is the rapid change in diatom assemblages during the last 20 y, indicating the onset of eutrophication. Limnological data from Lago de Zirahuen support this interpretation, although none are available from Laguna de Juanacatlan. Paleolimnology is a powerful tool in tracking recent change, particularly in the absence of regular limnological monitoring programs. These lakes appear to be highly sensitive to changes in catchment exploitation, which must be considered in future drainage basin management.
INTRODUCTION
The volcanic highlands of Central Mexico, or Trans-Mexican Volcanic Belt (TMVB), contain numerous lacustrine basins, many of which are hydrologically closed (Fig. 1). These have provided foci for human settlement for several thousand years and, as a result, many are experiencing considerable environmental degradation (1). Lake ecosystems are affected by increased soil erosion, nutrient enrichment, heavy metal pollution, and excessive groundwater abstraction (24). In addition, a trend toward drier climatic conditions since the 1970s has contributed to the lowering of some lake levels (46). Pioneering limnological work by De Buen on the lakes of Michoacan during the early 1940s (7, 8) provides a reference point for comparing results from recent investigations (9, 10), but such opportunities to examine long-term trends in water quality in Mexico are very rare. Effective management of water resources requires a longer temporal perspective to ascertain the impacts of anthropogenic and climatic stressors and an alternative approach is required. The application of paleolimnology as a tool for examining recent environmental change has become increasingly important in Europe and North America (11). Diatoms are particularly sensitive to changes in acidity and nutrient status. Diatom-based numerical reconstructions have provided insights into surface water acidification (12) and cultural eutrophication (13). A multiproxy approach is usually adopted, rather than relying on one line of evidence. For example, mineral magnetic properties can identify periods of enhanced soil erosion (14), whereas profiles of heavy metals in lake sediments have been used to examine the history of pollution from mining and smelting activity (15). The importance of paleolimnology in lake management is underlined by its inclusion in proposed methods for determining predisturbance reference conditions under the European Union Water Framework Directive (16). This study is part of a wider investigation into Late Holocene climate variability and human-environment interactions in central Mexico. Here, we focus on the historical sediment record (ca. 500 y) from two lakes: Lago de Zirahuen (Michoacan) and Laguna de Juanacatlan (Jalisco) (Figs. 1 and 2). Of particular signifcance is the most recent sedimentary record covering the last c. 20 years. Diatom analysis combined with magnetic suscepti-

Figure 1. Map of central Mexico illustrating major closed basins in the TMVB and location of the two study sites.

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 Figure 2. Photographs of a) Lago de Zirahuen and b) Laguna de Juanacatlan.

bility and heavy metal profiles help to elucidate the impacts of human activity on these catchments since at least the arrival of Spanish settlers in 1521. We demonstrate the value of paleolimnological records in providing an early warning signal of environmental degradation in Mexican lakes and suggest how this approach may be developed.

Study Area
Zirahuen Basin. Lago de Zirahuen (19826 0 N, 1018440 W) lies within a lava-dammed basin (Figs. 1 and 2) covering an area of 261 km2. The lake (approximately 10.5 km2) lies in the westernmost corner of the basin at 2075 m above sea level (a.s.l.) and is encircled by mountains reaching 3100 m a.s.l. Average annual temperature is 15.78C and average annual precipitation is 1182 mm yr1. Most precipitation (95%) falls in summer, between June and September. The natural vegetation of the basin is mixed pine and oak forest, although this is now largely restricted to steeper slopes due to clearance for settlement and agriculture. Lago de Zirahuen has a maximum depth of 40 m (mean depth 20.5 m). the lake has a pH of 8.4 and an electrical conductivity of 119 lS cm1 (17). It is classified oligo-mesotrophic, although the
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estimated phosphorus loading to the lake of 0.34 g m2 y1 (1996) suggests that lake waters of this closed basin should be richer in nutrients than has been measured (18). Reasons suggested for this discrepancy are: the sinking of cold, nutrient-rich inflowing water below the photic zone undergoing an apparent incorporation of chemical content to the lake bottom under aerobic conditions; negligible amounts of sulfur thus preventing phosphorus release from sediment; and that nitrogen and phosphorus may be colimiting, so eutrophication will only occur with increases in both nutrients (19). Despite the apparent lack of evidence for eutrophication, secchi disk transparency decreased by 23 m between 1987 and 1996 based on sampling data (9, 18). The two principal settlements in the basin, Santa Clara and Opopeo, both with populations greater than 10 000, are located on the main inflow to the lake, the R o de la Palma. On the lakeshore, the town of Zirahuen has a population of ;2000, and there are numerous small settlements. Santa Clara was an important center for copper smelting during the eighteenth century. Around this time, colonial settlers established haciendas (large, private agricultural enterprises) within the basin (20). Much land has now been cleared for agriculture (maize and wheat). In the last decade, a commercial fruit farm has been established on the south shore of the lake. Zirahuen is heavily promoted as a tourist attraction and accommodations have been built, including numerous private luxury homes. An exit from the recently constructed motorway to Uruapan was provided to encourage more visitors to the lake. Juanacatlan Basin. Laguna de Juanacatla n (20837 0 N, 104844 0 W), also a lava-dammed lake, is situated in a remote location in the Sierra de Mascota (Figs. 1 and 2). This small basin (approximately 10 km2) is oriented in a northwest to southeast direction. The lake occupies an area of approximately 0.5 km2 at the northwest end of the basin and lies at ;2000 m a.s.l. It is surrounded by steep slopes that rise to a maximum of 2300 m a.s.l. The closest meteorological station is at Mascota, some 800 m lower and 12 km away. Average annual temperature there is 21.88C, although temperatures at Juanacatlan are probably lower. Average annual precipitation at Mascota is 1026 mm y1 (21). The basin slopes are dominated by dense pine and oak forest. During the 1950s, an artificial exit channel was dug at the western end of the lake in order to provide irrigation water. In contrast to the Zirahuen Basin, there is no limnological monitoring program. Preliminary bathymetric measurements indicate a maximum depth of 25 m, but a detailed survey has not been undertaken. Data obtained in 1998 indicate that the lake has a pH of 8.8 and electrical conductivity of 148 lS cm1. Its ionic composition, like Zirahuen, is calcium-magnesium bicarbonate (17). In autumn 1998 and 2003, the lake was thermally and chemically stratified. The region was important for colonial gold and silver mining, with mines being exploited from the seventeenth century onward (22); these are no longer in operation. It was not possible to establish from historical records whether mining actually took place within the basin. The principal activity today is agriculture (maize and wheat cultivation and cattle farming). At the time of coring, settlement was restricted to small farming communities lying close to, but not within, the basin. Human impacts therefore appeared to be minimal. In September 1998, work began on a luxury tourist resort on the lakeshore aimed at attracting visitors and boosting the local economy. This development was completed in mid-2003.

MATERIALS AND METHODS

During March 1998, sediment cores (60 and 80 cm long) were obtained from both basins using a mini-Kullenberg corer. The sediment-water interface was captured. Cores were sealed, returned to the UK, and kept in cold storage at 48C. They were X-rayed, opened, and the visual stratigraphy described before sampling. Cores were analyzed at 4-cm intervals, with finer resolution sampling where major changes were identified. Mass

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specific magnetic susceptibility was measured. Metal concentrations were determined on HNO3/HCl digests of core sections using a Unicam SP9800 flame atomic absorption spectrometer (23). Concentrations of silver in Core JL/98 were determined by inductively coupled plasma optical emission spectrometry (ICPOES) using a Thermoelemental TJA IRIS instrument. Diatom samples were prepared using standard techniques (24) and at least 400 valves were counted in each sample. Species identification was carried out with reference to several published floras. Chronological control on cores from Lago de Zirahuen is provided by 210Pb dating, radiocarbon dating, and the identification of tephra layers from eruptions of Volcan Paricut n (A.D. 1943) and Volcan Jorullo (A.D. 17591764). This is discussed in detail elsewhere (25). Lead-210 dating and AMS radiocarbon dating were also used on cores from Laguna de Juanacatlan. Unfortunately, it was not possible to obtain a reliable 210Pb chronology for this site (discussed in more detail below). Results from the 1998 coring program at Juanacatlan are compared with those from a sedimentwater interface core (Core 1) obtained by R. Byrne (University of California at Berkeley) in 1990, on which diatom analysis was undertaken by S. Metcalfe. The chronology of Core 1 was established by combining 210Pb dates with laminae counting (Byrne, unpubl. data), a summary of which is presented here.

RESULTS AND INTERPRETATION Lago de Zirahuen The four cores obtained from Lago de Zirahuen revealed a spatially and temporally coherent record (25). Here, a summary of data from Core AV/98, taken in 12 m of water in the subbasin of Agua Verde, is presented, providing an overview of changes in the basin during the last ca. 500 y (Fig. 3). The core consists of grayish-brown and dark brown organic mud (gyttja), except for the uppermost 5 cm, which are oxidized reddish silt. This layer occurs across all the cores obtained and is likely the result of recent erosion of red soils around the lakeshore. An estimated age

of ca. A.D. 1550 was assigned to Core AV/98, based on extrapolation of 210Pb ages and comparison with historical tephra layers (25). Magnetic susceptibility is low between 58 and 50 cm, but rises steadily above this point, corresponding to the eighteenth century onward. The occurrence of the tephra from Volcan Jorullo helps to date a noticeable peak in the lead and copper profiles in the core. Although not highly pronounced, as the coring site lies at the farthest point from the surface inflow, these peaks indicate contamination from colonial smelting activity at Santa Clara. According to historical records, smelting operations peaked in 1789, diminishing greatly by the early twentieth century (26), although some coppersmiths continue to operate. Following the late-eighteenth century peak, copper concentrations remained slightly higher than those observed in the lower portion of the core, suggesting continued contamination. Prior to the mid-eighteenth century, the diatom flora of Lago de Zirahuen is dominated by small species of the genus Fragilaria, which are common in circum-neutral to slightly alkaline environments in central Mexico (27). However, the planktonic Cyclotella stelligera, which is found throughout the core in small amounts, increases in abundance through the latter half of the eighteenth century and is common until the 1970s. Diploneis elliptica, a species preferring slightly alkaline water (28), which is found in lakes, bogs, and springs, follows the same pattern. The ecology of Diploneis elliptica is not well documented, but Cyclotella stelligera is known to respond to increased phosphorus concentrations (29) and has been observed in horizons with increased mineral soil erosion (30). This distinctive change in diatom species composition coincides with the rise in magnetic susceptibility. Archival evidence indicates a marked increase in settlement and agricultural activity in the basin from the eighteenth century onward (20). Such activities, combined with deforestation to provide charcoal for copper smelting, would have enhanced soil erosion and increased nutrient inputs into the lake. Fine resolution diatom analysis has shown that the deposition of the Jorullo tephra did not

Figure 3. Core AV/98, Lago de Zirahuen, illustrating magnetic susceptibility, copper and lead profiles, and a summary of diatom species composition.

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have a significant impact on the diatom flora (31), so changes in the assemblage observed in the core cannot be attributed to this. Since the 1970s, the diatom flora has changed completely, with Cyclotella ocellata at relative abundances reaching ;80%. Also found in small amounts for the first time in the 500-y record is Fragilaria crotonensis. It is difficult to establish the ecology of Cyclotella ocellata from published literature and it has not been found in other lakes in central Mexico. Fragilaria crotonensis, however, is regarded as an indicator of eutrophication (32, 33). It appears that the diatom flora has responded dramatically and rapidly over a period of less than 10 y to recent land-use changes, including tourist development and commercial agriculture. The interpretation of a trend toward eutrophication is consistent with limnological observations. Although classified as oligo-mesotrophic, the phosphorus and inorganic nitrogen loading increased by 36% and 45% respectively, between 1987 and 1996, along with a reduction in secchi depth (18).

Laguna de Juanacatlan Core 1, retrieved in 1990 in c. 10 m of water, yielded a finely laminated sequence of millimeter-scale, alternating pale pink clay layers with greenish-brown organic layers (Fig. 4). It was presumed that these layers represent annual couplets, with clay layers representing wet season deposition of allochthonous material, but further monitoring is required to confirm this. Several thicker pink clay bands were identified, the most prominent occurring at a depth of 3639 cm. These have been interpreted as representing flood events resulting from tropical storms (Byrne pers. comm.). A chronological framework was established by Byrne (unpubl. data), indicating a basal age for the core of ca. A.D. 1520 and an age of A.D. 1820 for the clay layer. The diatom record is dominated by the planktonic Cyclotella stelligera throughout, forming up to 80% of the total (Fig. 4). Synedra acus and Synedra nana are present in significant numbers during the early part of the record until the late 1700s (52 cm). Also found in the lower portion of the core are Nitzschia palaecea and Nitzschia gracilis. From the late eighteenth century, Synedra

species are replaced by Aulacoseira granulata and its variety, angustissima. Small Fragilaria species also occur for the first time and the epiphyte Cocconeis placentula shows a slight increase in abundance. Previous research has shown that Synedra species have high silica and low phosphorus requirements and are the most effective competitors in systems with a limited phosphorus supply (34). Aulacoseira granulata and its varieties, however, have higher phosphorus requirements than Synedra. It is therefore likely that increased phosphorus availability from the late 1700s onward led to the change in the diatom assemblage. Three further cores were obtained in 1998 and showed a coherent pattern of change. Results from Core JL/98 obtained in 11 m of water are presented here (Fig. 5). The sequence was laminated except for two sections in the upper 15 cm. It was not possible to obtain a reliable 210Pb profile due to small sample size. Cesium-137 was present in the top 3 cm of core, but was not detectable in individual centimeter slices. This suggests that the top 3 cm represent the period after the 1963 weapons testing peak. Radiocarbon dates were obtained from a distinctive clay layer, thought to be correlative with that found in Core 1, and from 70cm depth, where the laminae composition changed toward more organic-rich layers. Calibrated age ranges of A.D. 14451636 and A.D. 13381495 (2r) were obtained for the clay layer and the compositional boundary, respectively (Table 1). These dates do not correspond to those estimated for Core 1, which may be the result of unreliable radiocarbon dates due to inwash of old carbon from the catchment, or errors in the Core 1 chronology. We can, however, agree that the sequence represents at least the last 500 y. Magnetic susceptibility is low throughout the core, but rises from 55 cm upward. A peak at 3637 cm corresponds to the pink clay layer. This layer also shows increased levels of silver, lead, and zinc. Below this layer, silver concentrations are below the detection limit (0.5 mg kg1) of the ICP-OES, a value of 12 mg kg1 being recorded within the layer itself. Above the layer, levels decline but remain higher than in the lower portion of core. The magnetic susceptibility and metal profiles indicate a significant catchment disturbance event, the date of which remains unclear.

Figure 4. Summary diatom diagram for Juanacatlan Core 1, retrieved in 1990. Dates are derived from a combination of laminae counting and 210Pb dating (Byrne, unpub. data).
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 Figure 5. Core JL/98, Laguna de Juanacatlan, illustrating magnetic susceptibility, selected heavy metals, and a summary of diatom species composition.
Table 1. AMS radiocarbon dates from Cores JL/98 and JD/98.
Core JL/98 JL/98 Depth (cm) 3637 6970 Laboratory Code AA-32323 AA-32324
14

C Age (61r)* 365 6 45 485 6 50

d13CPDB (60.1) 30.1 31.4

Calibrated Age Range (A.D.: 2r) 14451534 15381636 13171353 13881495 15011507 16011613

Rel. Area under probability distribution 0.487 0.513 0.082 0.903 0.005 0.011

14

C dates were produced by the University of Arizona AMS facility and calibrated using CALIB 4.1 (35).

The 14C date from JL/98 suggests that this may be the early colonial period, whereas Core 1 indicates a later age of 1820. The increase in silver from this point suggests that the initial disturbance may have been related to exploration for mineral resources. Unfortunately, historical records do not specify the locations of mines, but the town of Navidad, less than 10 km distant, was an important seventeenth century mining center. This time scale falls within the range of the calibrated radiocarbon date for the layer. The diatom record from JL/98 follows the same pattern of Core 1, with domination of Cyclotella stelligera throughout, and a switch from Synedra species to Aulacoseira granulata var. angustissima occurring slightly before the deposition of the clay layer. The species composition of the uppermost sediments, however, is completely different. Cyclotella stelligera is almost completely replaced by Fragilaria crotonensis, which accounts for more than 90% of the assemblage. As discussed earlier, this species is considered to be a eutrophication indicator. This dramatic change must have occurred some time between 1990 and 1998, indicating a very rapid response. In 1998, the catchment was not inhabited, but cultivation occurred along the flanks of the inflowing stream. It is not known whether any significant changes in agricultural practices have occurred since 1990.

DISCUSSION AND CONCLUSIONS Results from these two lakes show remarkably similar patterns. Both basins have experienced changes as a result of anthropo474

genic disturbance during the colonial period. In the Zirahuen Basin, accelerated soil erosion and nutrient enrichment from the mid-eighteenth century can be linked to increased anthropogenic activity recorded in numerous historical documents. Whereas similar events seem to occur in the record from Laguna de Juanacatlan, these cannot be conclusively attributed to human activity due to a lack of archival documents for the area. Metal profiles from both basins indicate contamination from colonial mineral exploitation. In Zirahuen, copper smelting during the eighteenth century resulted in increased copper and lead levels in core sediments. The timing and extent of colonial smelting operations at the town of Santa Clara are well documented from archival sources. It is likely that increased levels of silver in Juanacatlan Core JL/98 also result from colonial mineral exploitation, but due to problems with the core chronology and lack of supporting historical data, this cannot be confirmed. Diatom assemblages show a clear trend toward nutrient enrichment during the colonial period. The most dramatic feature though is the rapid, recent change in diatom flora, occurring in Zirahuen during the early 1980s and in Juanacatlan between 1990 and 1998. In both cases, composition changes completely, with species disappearing that had been present throughout the last several hundred years. The almost total dominance of Cyclotella ocellata in Zirahuen and Fragilaria crotonensis in Juanacatlan has led to a significant decrease in the diversity of the diatom flora in these lakes. The uppermost samples from the two lakes may represent individual blooms (which would account for their almost
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 monospecific nature), but plankton sampled at Juanacatlan in March and September 1998 consisted almost entirely of Fragilaria crotonensis, indicating that this species is dominant in both wet and dry seasons, whereas Cyclotella ocellata [previously recorded as C. kutzingiana (36)] has formed the dominant com ponent of Zirahuen phytoplankton samples since at least 1987. Limnological records do not exist for Laguna de Juanacatlan, but instrumental data from Lago de Zirahuen show a gradual trend toward eutrophication. Compared with many lakes in Mexico, Zirahuen is regarded as being in a pristine state (18); its clear, blue waters showing none of the telltale signs of nutrient enrichment. Subtle changes in nutrient concentrations in the water column are now being observed. Alone, these may not give cause for concern, but the lake sediment records that the aquatic biota has shown a major response. As tourist development increases in the basin, and the untreated sewage from the towns of Santa Clara and Opopeo continues to flow, the lakes buffering capacity against excess nutrient inputs is likely to be exceeded. It would be helpful to quantify the extent of nutrient enrich ment in both Juanacatlan and Zirahuen. In Europe and North America, successful reconstructions of total phosphorus have been produced using diatom-based transfer functions (13, 37). A calibration dataset for central Mexico has been developed (17), but focused on a salinity and alkalinity. A nutrient training set is now being developed by E. Hill (University of Nottingham). A quantitative approach will help to establish baseline conditions for Mexican water bodies, many of which are suffering considerable anthropogenic disturbance and will help assess the magnitude of recent eutrophication. Our paleolimnological study has shown that Lago de Zirahuen and Laguna de Juanacatlan have experienced increased disturbance during the colonial period, as a result of mineral exploitation and settlement. Historical records can contribute significantly to their interpretation. The diatom records highlight the sensitivity of lakes in the volcanic highlands of Mexico to anthropogenic activity. The recent, rapid response of the aquatic biota to environmental change is cause for concern and might have gone undetected. Our results demonstrate a need for more widespread monitoring of natural water bodies in Mexico, combined with analysis of recent lake sediment records. Together, these will help to inform decisions on drainage basin and water resources management in Mexico.
References and Notes
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Sarah Davies is a lecturer in the Quaternary Environmental Change research group at the Institute of Geography and Earth Sciences, University of Wales, Aberystwyth. Her address: IGES, University of Wales, Aberystwyth, SY23 3DB, UK. sjd@aber.ac.uk Sarah Metcalfe is professor of Earth and Environmental Dynamics in the School of Geography, University of Nottingham, University Park, Nottingham, NG7 2RD, UK. sarah.metcalfe@nottingham.ac.uk Fernando Bernal-Brooks is a researcher in the Instituto de Investigaciones Sobre Recursos Naturales at the Universidad Michoacana de San Nicolas de Hidalgo, Av. San Juanito s/n, Col. San Juanito Itzcuaro, Morelia, Michoacan. CP 58330, Morelia, Mexico. fbernal_brooks@yahoo.com Arturo Chacon is a researcher in the Instituto de Investigaciones Sobre Recursos Naturales at the Universidad Michoacana de San Nicolas de Hidalgo, Av. San Juanito s/n, Col. San Juanito Itzcuaro, Morelia, Michoacan. CP 58330, Morelia, Mexico. achacon@zeus.ccu.umich.mx John Farmer is professor of Environmental Geochemistry in the School of Geosciences, University of Edinburgh, Joseph Black Building, West Mains Road, Edinburgh, EH9 3JJ, UK. J.G.Farmer@ed.ac.uk Gus MacKenzie is a reader at the Scottish Universities Environmental Research Centre, Scottish Enterprise Technology Park, East Kilbride, G75 OQF, UK. A.MacKenzie@suerc.gla.ac.uk Anthony Newton is a research fellow in the School of Geosciences, University of Edinburgh, Drummond Street, Edinburgh, EH8 9XP, UK. ajn@geo.ed.ac.uk

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