Elsevier

Science of The Total Environment

Volume 532, 1 November 2015, Pages 40-47
Science of The Total Environment

Wading bird guano enrichment of soil nutrients in tree islands of the Florida Everglades

https://doi.org/10.1016/j.scitotenv.2015.05.097Get rights and content

Highlights

  • Tree island soil P concentration and δ15N values exceed other Everglades soils.

  • Characteristics of Everglades tree island soil may indicate guano deposition.

  • Deposition of stable guano P can exceed other P sources to tree island soil.

Abstract

Differential distribution of nutrients within an ecosystem can offer insight of ecological and physical processes that are otherwise unclear. This study was conducted to determine if enrichment of phosphorus (P) in tree island soils of the Florida Everglades can be explained by bird guano deposition. Concentrations of total carbon, nitrogen (N), and P, and N stable isotope ratio (δ15N) were determined on soil samples from 46 tree islands. Total elemental concentrations and δ15N were determined on wading bird guano. Sequential chemical extraction of P pools was also performed on guano. Guano contained between 53.1 and 123.7 g-N kg 1 and 20.7 and 56.7 g-P kg 1. Most of the P present in guano was extractable by HCl, which ranged from 82 to 97% of the total P. Total P of tree islands classified as having low or high P soils averaged 0.71 and 40.6 g kg 1, respectively. Tree island soil with high total P concentration was found to have a similar δ15N signature and total P concentration as bird guano. Phosphorus concentrations and δ15N were positively correlated in tree island soils (r = 0.83, p < 0.0001). Potential input of guano with elevated concentrations of N and P, and 15N enriched N, relative to other sources suggests that guano deposition in tree island soils is a mechanism contributing to this pattern.

Introduction

Determination of mechanisms controlling nutrient transport and transformations in soil is essential for wetland restoration planning and management. The Florida Everglades is a large (~ 10,000 km2), primarily freshwater wetland (Wetzel et al., 2005). Drainage and flood control projects constructed within the region resulted in the conversion of wetland habitat to agriculture and urban land uses (Davis, 1994, Light and Dineen, 1994, DeBusk et al., 1994). These projects, and subsequent nutrient loading, altered historic nutrient and hydrologic regimes in the region (DeBusk et al., 1994). Restoration activities are ongoing throughout the Everglades and mostly focus on water delivery and control of phosphorus (P), a limiting nutrient in this highly oligotrophic ecosystem. An area of marsh is described as P-enriched when soil total P concentrations exceed 500 mg kg 1 (McCormick et al., 1999, DeBusk et al., 2001).

The patches of trees and shrubs slightly elevated above the surrounding marsh are collectively described as tree islands (Sklar and van der Valk, 2002). Tree island soil P concentrations in the Everglades are reported to exceed the concentration of native marsh soil within the system, in some cases by two orders of magnitude or more (Orem et al., 2002, Wetzel et al., 2005, Ross and Sah, 2011).

Nutrient accumulation in tree island soil is primarily attributed to three mechanisms: evapotranspirational groundwater and surface water pumping by tree species, atmospheric deposition and deposition of animal waste (Wetzel et al., 2005, Ross et al., 2006). Accumulation of nutrients in tree island soils likely occurs at variable spatial and temporal scales among islands. If nutrient accumulation is variable among islands, differences could be attributable to the interactions between local surface and groundwater hydrologic gradients, differential vegetation patterns and wildlife distribution. Dramatic differences reported between tree island and marsh soils, and among tree island soils, may indicate that the mechanisms controlling P distribution between landforms may also influence distribution of P among islands. Soil P concentration of reconstructed tree islands, near the northern Everglades, was similar to marsh soil suggesting that tree island age may also play a role in soil nutrient accumulation (Rodriguez et al., 2014). Natural deposition or accumulation of P in high quantities may support an emerging theory for the ecology of the Everglades where high soil P and ecosystem health are no longer mutually exclusive (Wetzel et al., 2011).

Identification of P source is often challenging because of the complexity of P biogeochemistry. Wildlife species, particularly colonial nesting birds, have been described as potentially significant biovectors for nutrient transport, especially in the oligotrophic Everglades, and also in other wetland habitats (Bildstein et al., 1992, Frederick and Powell, 1994, Post et al., 1998). In the Everglades, wading birds generally forage in the emergent marshes and roost in patches of trees and shrubs dispersed throughout the ecosystem.

Spatial variation in foraging, and perching or nesting location within the ecosystem suggests a potential transport mechanism for nutrient redistribution (Frederick and Powell, 1994). Wading birds also seasonally nest in the Everglades in high density at many locations. Translocation of marine-derived nitrogen (N) and P to terrestrial island environments by seabirds, through guano deposition, is a mechanism for soil nutrient enrichment (Hutchinson, 1950, Anderson and Polis, 1999, Wait et al., 2005). Similarly in the Everglades, transport of nutrients, particularly N and P, from marsh-derived prey items through bird guano deposition has been hypothesized to influence the distribution of soil P throughout the ecosystem resulting in elevated soil P concentration in tree island soils (Orem et al., 2002, Wetzel et al., 2005). For example, large nesting aggregations of birds may be capable of importing metric tonnes of P annually (Frederick and Powell, 1994). Nutrient transport alone does not comprise a mechanism for nutrient accumulation, unless the deposited nutrients have been transformed to a relatively stable form.

Little is known about the magnitude of the hypothesized mechanisms that may control nutrient accumulation and distribution in tree island soil. Deposition of high P content animal wastes such as guano, dropped food or carcasses in natural ecosystem settings can occur in discrete locations such as nesting sites of avifauna. Frederick and Powell (1994) suggested that where Everglades wading birds nest in high density, P deposition by avifauna may approach 3000 times the atmospheric P deposition rate, thereby playing an important role in nutrient redistribution. Guano deposition by avian species is one of the primary hypotheses offered to explain high concentrations of P in Everglades tree islands (Wetzel et al., 2005, Wetzel et al., 2011). Birds have been associated with nutrient focusing in wetlands and on islands located in marine environments (Post et al., 1998, Anderson and Polis, 1999, Wait et al., 2005, Macek et al., 2009). Anderson and Polis (1999) reported seabird guano deposition elevated soil P concentration up to six times higher than unaffected soil. Although an investigation conducted by Wait et al. (2005) focused on N inputs from guano deposition, their data also indicated a ~ 18:1 difference in soil P observed in guano affected islands versus non-guano islands.

Determination of the P concentration and forms of P in wading bird guano from the Everglades may provide insight regarding a mechanism of P transportation, and fate of P, within the ecosystem. The transport of P by birds from marsh habitat to tree islands in the Everglades, and the subsequent accumulation of P in tree island soil have been suggested as a mechanism that contributes to the oligotrophic status of the marsh (Wetzel et al., 2005). Although nutrient transport by birds to islands in marine ecosystems has been well described, similar information for the Everglades is not widely available. Contribution of P derived from bird guano to tree islands may be reflected by similarities between chemical properties of soil and guano. The purposes of this study were to: (1) chemically characterize wading bird guano collected from the Everglades, (2) investigate tree island soil characteristics and correlations among properties, and (3) estimate mass deposition of nutrients at Everglades tree islands from guano.

Section snippets

Site locations, descriptions and sample collection

Soil was collected from 46 tree islands between 2005 and 2011 in the central and southern Everglades, Florida, USA (Fig. 1). All soil samples were collected from the head region of the tree island, which is the location most likely to have the highest concentration of soil P (Wetzel et al., 2009). The samples were oven-dried, and passed through a 2 mm mesh sieve prior to analysis. Soil samples were collected from depths ranging from of 0–5 cm (n = 17) and 0–10 cm (n = 29). These sampling depths were

Guano characterization and deposition

Guano pH was near neutral, and based on dry weight was 23% C (Table 1). Total Ca, N and P cumulatively comprised approximately 30% of the guano mass (Table 1). In addition to Ca, N and P comprising a relatively large proportion of the guano, it was enriched in 15N relative to atmospheric N and the δ15N signature varied among samples ranging from 7.8 to 10.6‰ (Table 1; Irick, 2012, Zhu et al., 2014). The combined concentrations of total Al, Fe, K and Mg in the guano samples on average accounted

Discussion

Guano deposition is one of the three main hypotheses explaining elevated P in tree island soil (Wetzel et al., 2005). Guano pH was similar to the range reported for seabird guano, and samples of poultry manure and litter (Gillham, 1956, Codling, 2006, Dail et al., 2007). The range of organic matter content observed in the guano may indicate different proportions of urine and fecal matter present in different samples of guano because avian excrement consists of two parts: fecal matter and urine.

Conclusion

This work provides new insight toward the guano contribution hypothesis by characterizing a P source to tree island soil and elucidating an isotopic indication of P source. Bird guano had high concentrations of P and N, and the guano N is enriched in 15N. Approximately 90% of P deposited as guano was a relatively stable (HCl extractable or residual) form derived from consumed biomass, which could accumulate in tree island soil. Deposition of stable guano P and 15N enriched N can occur at rates

Acknowledgments

The authors would like to thank Ms. Guiqin Yu, and Drs. Kathy Curtis, Yigang Lou and Shengsen Wang for their help with this work. We also thank the staff of Ecology and Environment, Inc. and the staff of Dr. Michael Ross's lab for sample collection.

References (60)

  • D.A. Wait et al.

    Seabird guano influences on desert islands: soil chemistry and herbaceous species richness and productivity

    J. Arid Environ.

    (2005)
  • Y. Zhu et al.

    Wading bird guano contributes to Hg accumulation in tree island soils in the Florida Everglades

    Environ. Pollut.

    (2014)
  • W.B. Anderson et al.

    Nutrient fluxes from water to land: seabirds affect plant nutrient status on Gulf of California islands

    Oecologia

    (1999)
  • A.L. Bates et al.

    Preliminary use of uric acid as a biomarker for wading birds on Everglades tree islands, Florida, United States

  • K.L. Bildstein et al.

    The relative importance of biotic and abiotic vectors in nutrient transport

    Estuaries

    (1992)
  • M.I. Bird et al.

    Stable carbon and nitrogen isotope analysis of avian uric acid

    Rapid Commun. Mass Spectrom.

    (2008)
  • E.E. Codling

    Laboratory characterization of extractable phosphorus in poultry litter and poultry litter ash

    Soil Sci.

    (2006)
  • M.J. Cohen et al.

    Reciprocal biotic control on hydrology, nutrient gradients and landform in the greater Everglades

    Crit. Rev. Environ. Sci. Technol.

    (2011)
  • C.B. Craft et al.

    Peat accretion and phosphorus accumulation along a eutrophication gradient in the northern Everglades

    Biogeochemistry

    (1993)
  • C.L. Coultas et al.

    Petrocalcic horizon formation and prehistoric people's effect on Everglades tree island soils, Florida

    Soil Surv. Horiz.

    (2008)
  • H.W. Dail et al.

    Effect of drying on phosphorus distribution in poultry manure

    Commun. Soil Sci. Plant Anal.

    (2007)
  • S.M. Davis

    Phosphorus inputs and vegetation sensitivity in the Everglades

  • W.F. DeBusk et al.

    Spatial Distribution of Soil Nutrients in a Northern Everglades Marsh: Water Conservation Area 2A

    Soil Sci. Soc. Am. J.

    (1994)
  • W.F. DeBusk et al.

    Spatiotemporal patterns of soil phosphorus enrichment in Everglades Water Conservation Area 2A

    J. Environ. Qual.

    (2001)
  • D.A. Frank et al.

    The role of ammonia volatilization in controlling the natural 15N abundance of a grazed grassland

    Biogeochemistry

    (2004)
  • P.C. Frederick et al.

    Nutrient transport by wading birds in the Everglades

  • T. Fukami et al.

    Above- and below-ground impacts of introduced predators in seabird-dominated island ecosystems

    Ecol. Lett.

    (2006)
  • M.E. Gillham

    Ecology of the Pembrokeshire Islands: V. Manuring by the colonial seabirds and mammals, with a note on seed distribution by gulls

    J. Ecol.

    (1956)
  • B. Gu et al.

    Mercury and sulfur environmental assessment for the Everglades

  • D.J. Hawke et al.

    Mobilisation of recalcitrant soil nutrient fractions supports foliar nitrogen to phosphorus homeostasis in a seabird soil

    Plant Soil

    (2014)
  • D.J. Hawke et al.

    Inventories and elemental accumulation in peat soils of forested seabird breeding islands, southern New Zealand

    Aust. J. Soil Res.

    (2004)
  • Z. He et al.

    Phosphorus distribution in sequentially extracted fractions of biosolids, poultry litter, and granulated products

    Soil Sci.

    (2010)
  • A.H.M. Hieltjes et al.

    Fractionation of inorganic phosphates in calcareous sediments

    J. Environ. Qual.

    (1980)
  • G.E. Hutchinson

    Survey of contemporary knowledge of biogeochemistry. 3. The biogeochemistry of vertebrate excretion

    Bull. Am. Mus. Nat. Hist.

    (1950)
  • D.L. Irick et al.

    Characteristics of soil phosphorus in tree island hardwood hammocks of the southern Florida Everglades

    Soil Sci. Soc. Am. J.

    (2013)
  • Irick, D.L., 2012. Soil phosphorus characteristics and sources in tree islands of the Florida Everglades. Dissertation,...
  • P.W. Inglett et al.

    Stable C and N isotopic ratios of macrophytes as an indicator of wetland eutrophication: patterns in the P-affected Everglades

    Limnol. Oceanogr.

    (2006)
  • P.W. Inglett et al.

    Increased soil stable nitrogen isotopic ratio following phosphorus enrichment: historical patterns and tests of two hypotheses in a phosphorus-limited wetland

    Oecologia

    (2007)
  • Y.M. Kuo et al.

    Apatite control of phosphorus release to runoff from soils of phosphate mine reclamation areas

    Water Air Soil Pollut.

    (2009)
  • R.G. Leighty et al.

    Soil survey (detailed-reconnaissance) of Dade County, Florida

  • Cited by (28)

    • Positive feedbacks between savanna tree size and the nutritional characteristics of “Islands of fertility” are amplified by sociable weaver colonies

      2023, Journal of Arid Environments
      Citation Excerpt :

      High levels of P, K, Ca, and Zn under the nest-tree soils imply that plants can benefit from the abundant N under the nest-trees. Furthermore, the higher concentrations of P, K, Ca, and Zn that we found are consistent with other studies on soils associated with colonial birds (Hobara et al., 2005; Breuning-Madsen et al., 2010; Zwolicki et al., 2013; Irick et al., 2015; Otero et al., 2018). However, the stoichiometric ratios of constituent elements in the sociable weaver faecal matter have very different ratios to the soils below nest-trees.

    • Use of a wastewater recovery product (struvite) to enhance subtropical seagrass restoration

      2022, Science of the Total Environment
      Citation Excerpt :

      DOC and TDN samples were analyzed on a Shimadzu TOC-L analyzer fitted with a N module (Shimadzu Scientific Instruments, Durham, NC, USA) according to EPA method 415.1 for TOC and ASTM D 8083 for total nitrogen (TN) (ASTM International, 2016; Nevins et al., 2020; USEPA, 1974). TDP was digested with persulfate in an autoclave and analyzed via a Shimadzu UV-1800 spectrophotometer (Shimazdu Corporation, Kyoto, Japan) using EPA method 365.1 (Irick et al., 2015; USEPA, 1993). At the end of the experiment, plant biomass and sediment were destructively sampled.

    • Nutrient cycling

      2022, Fundamentals of Tropical Freshwater Wetlands: From Ecology to Conservation Management
    View all citing articles on Scopus
    View full text