Earthworm abundance and nitrogen mineralization rates along an urban-rural land use gradient

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Soil Bid. Eiochem.Vol.29, No. 314, pp. 427430, 1997 0 1997 Elsevicr Science Ltd. All rights reserved Printed in Chat Britain soo38-@717(%)oo@43-0 0038-0717197 $17.00+0.00

EARTHWORM ABUNDANCE AND NITROGEN MINERALIZATION RATES ALONG AN URBAN-RURAL USE GRADIENT

LAND

DAVID A. STEINBERG,’ RICHARD V. POUYAT,2* ROBERT W. PARMELEE) and PETER M. GROPFMAN’ ‘Instituteof Ecosystem Studies, Mary Flagler Cary Arboretum, Box AB, Millbrook, NY 12545, U.S.A., USDA Forest Service, Northeastern Forest Experiment Station, c/o Institute of Ecosystem Studies, Box AB, Millbrook, NY 12545, U.S.A., ‘and Department of Entomology, 1735 Neil Ave., Ohio State University, Columbus, OH 43210, U.S.A.

(Accepted 11 January 19%) Summary-FVeliminary observations of glaciated regions in North America suggest that forest stands associated with urban areas may support high populations of non-native species of earthworms relative to forests in rural areas. Moreover, the presence of these non-native species of worms may be moderating the effects of pollutant deposition on litter quality, or the decomposability of litter, and subsequently nutrient cycling processes in the urban stands. In this study we quantified earthworm abundance and biomass in urban and rural oak forest stands along a 130 x 20 km urban-rural transect in New York City, USA metropolitan area. We also evaluated the effects of earthworms on potential net N mineralization and nitrification in a laboratory microcosm study. Earthworm abundance and biomass along the transect was significantly higher in urban (25.1 individuals me2 and 2.16 g m-*) than in rural (2.1 individuals m-* and 0.05 g m-*) stands. In a microcosm study, potential net N mineralixation rates (0.15 mg N kg-’ d-‘) were significantly higher in urban soil with earthworms than in urban soil without earthworms, which exhibited a net immobilization of N. Rural soil with earthworms had significantly higher rates (0.57 mg N kg-’ h’) than urban soil with earthworms and rural soil without earthworms (0.28 mg N kg-’ h’). Nitrification rates in urban soils were surprisingly high given the relatively low litter quality and rates of N mineralization in these soils. The results suggest that earthworms may play an important role in forest ecosystems embedded within urban areas by enhancing nitrogen cycling processes and thereby compensating for the effects of air pollution on litter quality and de-

composition. 0 1997 Elsevier Science Ltd

INTRODUCTION A 130 km long, 20 km wide transect running from New York City to western Connecticut has been established to examine various responses of forest ecosystem sttucture and function to environmental factors along an urban-rural land use gradient (McDonnell et al., 1993; Pouyat et al., 1995). Pouyat et al. (1995) reported that N mineralization and nitrification in the A horizon soil of oak stands were higher at the urban than at the rural end of the gradient, despite the fact that leaf litter quality, a factor that usually strongly influences rates of N mineralization, was significantly lower at the urban end of the gradient. In another study along the transect, earthworm cast counts showed that earthworms were abundant in stands at the urban end of the gradient but were generally absent from stands at the rural end of the gradient (R. V. Pouyat, unpubl. PhD thesis, Rutgers University, 1992). Barthworms can strongly influence rates and patterns of N mineralization (Scheu, 1987; Blair et al., 1995), so that differences in earthworm activity at opposite *Author for correspondence (fax: 914 677 5976).

ends of the transect may contribute to the observed differences in N mineralization rates. Therefore, this study was designed to determine whether earthworm activity contributes to the high rates of N mineralization measured in the soil A horizon at the urban end of the gradient, despite the presence of lower quality leaf litter. Our objectives were (1) to measure earthworm abundance in oak stands along the transect, and (2) to measure the effects of earthworms on potential net N mineralization and nitrification in laboratory microcosms.

MATERIALSANDMETHODS The urban-rural transect encompasses an area of similar surface geology made up of contrasting land use types, extending from Bronx County, New York, through sites in Westchester County, New York, to Litchfield County, Connecticut (Pouyat et al., 1995). In a previous study, nine oak stands were grouped by threes into three land use types to provide a reasonable approximation of urban, suburban and rural envitonments along the transect (Pouyat et al., 1994). At each stand, one of three originally established plots was ran-

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domly selected for the abundance and biomass surveys. Each study area consisted of a 45 m transect located adjacent to the corresponding plot. Ten 25 x 25 cm quadrats were established at 5 m intervals along each transect, for a total of 30 sample quadrats for each land use type (90 total quadrats). Earthworms were collected using hand-sorting to a depth of 20 cm followed by the addition of a dilute (0.25%) formalin solution (Lee, 1985). All earthworms were counted, weighed and identified to family and in some cases species (specimens not identifiable to species were preserved for later identification). Abundance is expressed as numbers m-* and biomass data is presented as g ash-free dry mass m-* (AFDM). The microcosm study consisted of a 2 x 2 factorial design incorporating two soil environments (urban and rural) and two earthworm densities (with or without earthworms). The microcosms were established in 1 quart Mason jars. Soil for the microcosms was gathered during the earthworm survey from the A horizon, frozen for 24 h to kill earthworm cocoons, and allowed to thaw to room temperature. Litter was then added to the microcosms at levels approximating those found in the field (3 g per microcosm or 70 mg cm-*) and separated from the soil by 0.5 x 0.5 cm nylon mesh. Juvenile earthworms of the species Amynthas huwuyunus were added to each of 12 microcosms at a fresh weight roughly equivalent to maximum biomass levels measured in the survey (approximately 40 mg per microcosm). To simulate field conditions, the jars were stored at a constant 15°C on a 12 h light-dark cycle with sides covered. Soil moisture was adjusted to keep

al

moisture levels consistent across treatments. The incubation ran for 26 d. Two soil samples were removed for analysis from each microcosm at days 1, 13 and 26 using a microcoring device (7 mm dia) after a conditioning period of 7 d. Each sample hole was immediately backfilled with soil as the samples were taken. To determine NH; and NO; concentrations, soil samples were extracted with 2~ KC1 using procedures described in Pouyat (unpubl. PhD thesis, 1992).

RESULTS earthworm density was significantly Average (P < 0.05) higher in urban land use types (25.0 individuals m-*) than in rural types (2.5 individuals m-*), while suburban land use types were intermediate in number (7.0 individuals m-*). Likewise, average earthworm AFDM was significantly (P< 0.05) higher in urban land use types (2.16 g m-*) than in rural types (10 mg m-*), with suburban stands exhibiting intermediate amounts of biomass (50 mg m-‘). The most abundant earthworms in the urban stands were from the family Megascolecidae (A. agrestis and A. hawayanus). The lumbricids (Lumbricus rubellus and Dendrobaem octuedra) were also present. Based on the occurrence of surface casting, earthworms appeared to be active for the entire incubation period (pers. observ.). Earthworm activity increased potential net N mineralization in soils from both urban and rural environments (Fig. 1). Urban microcosms with earthworms exhibited an average potential net N

Rural

Urban

Soil Type Fig. 1. Mean ( + SE) potential net N mineralization over a 26 d incubation period for urban and rural soil environments. Potential net N mineralization is expressed as a change in the sum of NH:-N plus NOT-N over 26 d. Shaded bars represent earthworm addition treatments and unshaded bars represent non-earthworm treatments. Each bar is the mean of six replicates.

Earthworm effects on N dynamics in urban forest soils

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Rural

Urban

Soil Type Fig. 2. Mean ( + SE) potential net nitrification over a 26 d incubation period for urban and rural soil environments. Potential net nitrification is expressed as the change in NOT-N over 26 d. Shaded bars represent earthworm addition treatments and unshaded bars represent non-earthworm treatments. Each bar is the mean of six replicates. mineralization of 3.88 mg total inorganic N kg-’ soil (SE = 1.48 mg kg-‘). Conversely, urban microcosms without earthworms showed a net immobilization of

3.61 mg inorganic N kg-’ (SE = 0.95 mg kg-‘). Rural microcosms with earthworms showed a net mineralization of 14.73 mg total inorganic N kg-’ (SE = 5.05 mg kg-‘), while rural microcosms without earthworms showed a net mineralization of 7.33 mg inorganic N kg-’ (SE = 1.28 mg kg-‘; Fig. 1). The potential net N mineralization rate was significantly different between soil types (P=O.O02) and between earthworm treatments (P = 0.022). All microcosms showed an increase in NO?-N over the course of the study (Fig. 2). However, only in urban soil microcosms did earthworms have a positive effect on potential net nitrification. Urban soils without earthworms, rural soils with earthworms, and rural soils without earthworms showed net increases of mg NOT-N kg-’ of 4.48 ( + 1.09), 3.09 ( f 0.42) and 3.86 ( + 0.36), respectively (Fig. 2). The urban soil with earthworms showed a 2- to 3-fold increase in net accumulation of NOT-N over that in urban soil without earthworms (Fig. 2). Potential net nitrification rates differed significantly between soil treatments (P = 0.013), between earthworm treatments (P=O.O21), and for the soil x earthworm interaction term (P = 0.046). DISCUSSION The earthworm densities measured in this study fall within the range found in the literature for deciduous forests in North America. Reynolds (1970, 1972) reported densities ranging between 2 and 124 individuals m-’ of Lumbricidae in deciduous stands in

Tennessee and Indiana compared to 2.5 and 25 individuals m-’ measured among the oak stands sampled in this study. Why earthworm abundance is higher at the urban

end than at the rural end of the land use gradient is open to speculation. Pliocene glaciation destroyed a large portion of the oligochaete earthworm population in northern North America (Gates, 1976). The lack of earthworms in the rural sites supports this view. However, the existence of peregrine species of earthworms in the urban forest stands suggests that the introduction of exotic species was more intense and persistent at the urban end of the transect. Gates

(1976) has suggested that lumbricids and megascolecids were accidentally introduced from the ballasts of ships and in soil accompanying imported plants originating from Europe and Asia. As New York City served as an important international seaport, earthworm introduction probably occurred early and repeatedly in New York City’s history. The persistence of these non-native species in urban stands may be attributable to the proximity of these stands to highly maintained landscapes such as gardens, lawns and refuse sites. Once introduced, peregrine earthworm species are well-suited to these human-modified habitats (Lee, 1985), which can serve as sources of colonizing earthworms. Moreover, earthworm productivity and activity in urban stands may be linked to increased N availability in urban stands as a result of chronic N deposition. Satchel1 (1980) regarded N content of food resources as the critical limiting factor for earthworm persistence in heathlands and experimental birch plots in England. Since earthworm reproductive rates tend to rise with temperature (van Giestel et al., 1992) and metabolic rates also may

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increase.

the urban

“heat

island”

effect

mav influence I

by prolonging their period of activity and increasing production of biomass. Whether these results are typical for all urban and suburban areas needs to be tested in future studies. Our study demonstrates that earthworms have the potential to stimulate N mineralization in forest soils along this urban-rural land use gradient. The presence of earthworms in urban soil microcosms led to a switch from net immobilization to a net mineralization of N. The presence of earthworms in rural soil microcosms had the effect of doubling potential net N mineralization (Fig. I). Overall rates of potential net N mineralization were significantly higher in rural microcosms than in urban microcosms, a result that would be expected based on studies that have shown that litter quality is lower in urban than in rural stands (Pouyat et al., 1995). However, the difference between the two soil environments that most closely approximate field conditions (i.e. urban soils with earthworms and rural soils without earthworms) was smaller than the difference between the urban and rural soils without worms. With the added effects of the urban heat island and inputs of exogenous N from deoosition. overall rates of N min. eralization in urban soils may approach rural rates under field conditions. This result should be tested with field manipulations in future studies. Rates of nitrkcation in urban soils were surprisingly high given the low rates of mineralization in these soils. Nitrification in forest soils is strongly controlled by the supply of NH: from mineralization (Vitousek, 1981). The strong nitrification response to earthworms in the urban soils suggests that worms may play an important role in overcoming the effects of low mineralization on nitrification in these soils. In urban soils, earthworms may be altering competitive interactions for NH; by creating microsites in soil where plant and heterotrophic microbial demand for NH: is low, allowing nitrifiers to obtain NG despite low rates of mineralization. Moreover, the urban forest soils may have higher abundances of nitrifying bacteria than rural sites because of consistently high rates of earthworm activity or chronic deposition of N, both of which could result in reduced heterotroohic activitv (particularly from fungi) and a relatively consisteit supply of NH;. Indeed, Pouyat et al. (1994) found lower litter fungal abundances in the urban sites than in the rural sites used in this studv. Additionallv. there is evidence that earthworms affect the availability of N through their effects on microbial activity. Blair et al. earthworms

2

(1997)

found

that earthworms

decreased

microbial

bio-

mass in field microcosms. which had the effect of increasing rates of nitrification. Otherwise, little is known about earthworm effects on microbial biomass, microbial immobilization of N and nitrification in forest soils.

Acknowledgements-We

thank P. Bohlen for his comments and suggestions on this manuscript and S. James for identifying earthworm species. W. Turechek provided valuable assistance with field sampling. Funding- support came from a National Science Foundation, the U.S. Forest Service. Northern Global Change Program and the Northeastern Forest Experiment Station Research Unit NE-4952, Syracuse, New York. This is a contribution to the programme of the Institute of Ecosystem Studies.

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