Elsevier

Acta Oecologica

Volume 105, May 2020, 103580
Acta Oecologica

Assessing the influence of riparian invasion by the shrub Lonicera maackii on terrestrial subsidies to headwater streams

https://doi.org/10.1016/j.actao.2020.103580Get rights and content

Highlights

  • In areas of heavier invasion of Amur honeysuckle (L. maackii) there was less coarse woody debris.

  • In areas of heavier invasion of Amur honeysuckle (L. maackii) there was less fine woody debris

  • These results indicate linkage between invasion and terrestrial subsidies mediated through the physiognomy of the shrub.

  • Riparian invasion of L. maackii may alter the biology of streams through modification of allochthonous organic matter.

Abstract

Invasion of Amur honeysuckle (Lonicera maackii) into riparian areas of headwater streams creates strong potential for alterations of terrestrial subsidies that may drive bottom-up effects on aquatic biota. In this study, we analyzed effects of L. maackii on terrestrial subsidies in stream sites that represented a gradient of invasion intensity in temperate deciduous forests of southwestern Ohio (USA). Leaf litter biomass, terrestrial and aquatic fine woody debris (0.5–9.9 cm diameter) volume and count, and terrestrial and aquatic coarse woody debris (>9.9 cm diameter) volume were analyzed. Based on previous research, we hypothesized that sites with a higher density of L. maackii would have decreased native species subsidies due to the dense overarching structure of the invasive shrub preventing materials from entering the stream. Over the course of the study, we found no evidence of differences in native leaf biomass across the invasion gradient. There were marginally significant effects of invasion level on fine woody debris, and regression analysis revealed a significant (R-squared 0.11; P = 0.043) negative relationship between L. maackii stem density and fine woody debris volume. Coarse woody debris volume was lower in sites with heavier invasion although no statistically discernible effects were detected. Regression analysis indicated a statistically significant negative relationship between L. maackii basal area and coarse woody debris volume (R-squared 0.14; P = 0.026). These results indicate linkage between invasion intensity and terrestrial subsidies mediated through the unique physiognomy of the invasive shrub. Riparian invasion of L. maackii may alter the fundamental biology of streams through alterations to deposition of terrestrial organic matter that serves as a structuring component of smaller waterways.

Introduction

The biology of small streams is connected to the surrounding landscape through organic matter subsidies. Riparian vegetation is a particularly important contributor of subsidies to aquatic habitats and the amount and quality of organic matter input is critical to aquatic biota as these materials are a source of food and habitat (Vannote et al., 1980; Sweeney et al., 2004). In fact, much of the energy accessible to in-stream biota comes from terrestrial organic inputs (Fisher and Likens, 1973). Leaf material is an essential resource for aquatic biota and, in temperate climates, autumnal deposition from deciduous trees is particularly important to the ecology of headwater streams (Vannote et al., 1980; Wallace et al., 1997). Fine and coarse woody debris are subsidies that are fundamental to stream biology as these materials provide a variety of ecological functions including creating habitat complexity and providing substrata for biofilm formation (Benke et al., 1985; Ward and Aumen, 1986). Woody debris has been shown to strongly influence the diversity, abundance, and biomass of aquatic species (Benke et al., 1985; Wallace et al., 1997). Alterations to subsidies that influence macroinvertebrate communities can have bottom-up effects influencing higher trophic levels (Baxter et al., 2005). Riparian zones are subject to myriad disturbance processes of both natural and anthropogenic origin and these alterations have strong potential to shift the quality and quantity of terrestrial subsidies (Nilsson and Svedmark, 2002).

Riparian invasion by exotic plants has strong potential to alter riparian ecosystem function and shift the composition and quality of cross-system material subsidies. Indirect effects of invasive species may occur when pests or pathogens cause transformation of the riparian vegetation by inducing mortality among important species. For example, invasion of the exotic fungal pathogen Cryphonectria parasitica caused loss of American chestnut (Castanea dentata) and replacement by oaks (Quercus spp.) which have leaves with lower nutritional quality, thus leading to effects on macroinvertebrate shredders (Smock and Macgregor, 1988). Direct effects of invasive species are also possible and are particularly likely when the exotic species has traits that are unique to the invaded habitat. For instance, invasive species may have higher foliar nitrogen content (Leishman et al., 2007) which may influence nutrient cycling through increased decomposition rates (Ashton et al., 2005). Deposition of leaf material from the terrestrial environment into streams by riparian Russian olive (Elaeagnus angustifolia) was shown to increase the amount of dissolved organic nitrogen in streams thus altering nutrient cycling (Mineau et al., 2011). In addition to foliage, alterations to riparian vegetation have strong potential to influence in-stream fine woody debris (FWD) and coarse woody debris (CWD) which are key components of habitat structure especially in smaller streams (Vannote et al., 1980). Effects on CWD have been linked to changes in riparian vegetation associated with invasion by exotic species (e.g.,Tabacchi and Planty-Tabacchi 2003). Invasive species are known to thrive in disrupted habitats (Mack and Antonio, 1998; Huston, 2004), making riparian forests particularly vulnerable to ecological invasion.

The terrestrial shrub Lonicera maackii was introduced to the United States from Asia for horticulture reasons and has become a significant invasive species in many parts of eastern North America (Luken and Thieret, 1996). Lonicera maackii can create dense stands which have wide-ranging impacts on the biology of the invaded systems (Peebles-Spencer et al., 2017; McNeish and McEwan, 2016; Woods et al., 2019). McNeish and McEwan (2016) present a broad framework for L. maackii effects on both terrestrial and aquatic habitats including a hypothetical link between terrestrial invasion and stream macroinvertebrate communities mediated through alterations in organic matter deposition. Foliage from L. maackii has a unique chemical composition in relationship to native species (Arthur et al., 2012) and previous work has indicated negative effects on terrestrial insect herbivores (McEwan et al., 2009b; Lieurance and Cipollini, 2012, 2013). Evidence suggests that submerged leaf litter, fruits and flowers from L. maackii can create toxic conditions for aquatic macroinvertebrates (Custer et al., 2017; Borth et al., 2018). The invasion of L. maackii into forests surrounding headwater streams has potential for alterations of the riparian physiognomy generating a dense canopy above the stream (bottom panel, Supplemental Fig. 1). In a restoration experiment, the removal of L. maackii was associated with increased leaf organic matter deposition into a headwater stream (McNeish et al., 2015). This effect was hypothesized to be linked to the physical structure of the invasive shrub and McNeish et al. (2015) posit that the canopy of L. maackii represents a physical barrier that traps or deflects falling leaves, altering autumnal deposition. The McNeish et al. (2015) postulate regarding native leaf litter remains untested and, if the dense physiognomy creates a filter effect on native leaves, there is strong possibility for effects on other organic matter subsidies such as FWD and CWD.

In this study, we sought to test the hypothesis that terrestrial-to-aquatic subsidies are altered by the invasion of L. maackii into riparian areas surrounding headwater streams in temperate deciduous forests. This study took place on a set of headwater streams that represent a gradient of L. maackii invasion intensity that ranged from heavy (HVY) to moderate (MOD) invasion and sites without invasion which we considered reference conditions (REF) (Supplemental Fig. 1). Assessment of cross-habitat subsidies included measuring leaf litter and both fine and coarse woody debris. Following the McNeish et al. (2015) observation of lower foliar biomass in areas with L. macckii present, we hypothesized that (H1) sites with a higher invasion density would have decreased total leaf litter biomass deposition. Based on the intentionally established gradient of sites, we also expected L. maackii leaf biomass would increase as invasion intensity increased, and due to its extended leaf phenology (McEwan et al., 2009a), we anticipated a pulse of L. maackii litter later in the season than native species. We also sought to test the hypothesis that woody biomass in the form of both fine woody debris (H2) and coarse woody debris (H3) would decrease along the invasion gradient.

Section snippets

Establishing the experimental Lonicera maackii gradient

This study was focused on a set of five headwater streams and the surrounding riparian zones in the Miami Valley of southwestern Ohio, USA. These were 1st or 2nd order streams that were similar in terms of sinuosity, discharge, size and surrounding land-use. They had no apparent anthropogenic influence from adjacent activities including agriculture or suburban land development and were surrounded by a buffer of forest. The riparian forests were relatively similar across the sites and were

Results

Analysis of L. maackii stems indicated that the study gradient represented a wide range of stem density. Lonicera maackii was effectively absent from the reference sites (REF.A and REF.E) and the number of both live and dead stems present was significantly lower than the other sites in the study (P < 0.01 for all; Fig. 2). The moderate invasion sites (MOD.E and MOD.C) had significantly higher density than the reference sites, but were indistinguishable from the heavy invasion site (HVY.B; Fig. 2

Influence of L. maackii invasion on leaf litter in headwater streams

Invasion by L. maackii into forests has significant implications for the biology of forests (Collier et al., 2002; Miller and Gorchov, 2004; Peebles-Spencer et al., 2017; Woods et al., 2019) and the headwater streams that meander through those forests (McNeish et al., 2012, Custer et al., 2017). McNeish et al. (2015) found that riparian forest removal of L. maackii was associated with increasing leaf biomass from the native overstory canopy leading to the hypothesis that the physiognomy of the

Summary

In summary, invasion of riparian habitats by L. maackii has strong potential to influence subsidy transfer from terrestrial habitats into headwater streams. We found no evidence of reduced leaf litter from native trees entering streams in areas with heavy L. maackii invasion, (refuting H1); however, the late senescence and unique chemistry of the L. maackii leaf input may be a novel subsidy impacting aquatic biota. We found evidence to suggest that fine woody debris was reduced by L. maackii

Author contribution

Erin Rowekamp and Ryan McEwan designed the study. Erin Rowekamp led and executed field sampling, lab sample processing and other data collection and entry processes. Erin Rowekamp, Julia Chapman and Ryan McEwan conducted data analysis. Erin Rowekamp and Ryan McEwan wrote the manuscript.

Acknowledgements

The authors wish to express our gratitude to the Five Rivers Metroparks and Miami County Park district for allowing us access to research sites. We thank many different members of the McEwan Lab who participated in conceptualization, data collection or provided helpful ideas and comments including Eric Borth, Caitlin Buchheim, Taylor Buskey, Shante Eisele, Sarah Frankenberg, Angela Giaquinto, Corey Kuminecz, Sean Mahoney, Meg Maloney, Kyle McGeary, Joesph Murphy, and Charlotte Shade. The

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