Printer Friendly

Consumption of native green ash and nonnative common buckthorn leaves by the amphipod gammarus pseudolimnaeus.


Research on the functional implications of global changes to riparian plant communities reviewed by Kominoski et al. (2013) predicts alterations to hydrologic regimes, reductions in biodiversity and loss of functional redundancy. Additionally, changes to the quality, quantity, and timing of litter inputs to both terrestrial and aquatic systems are expected to alter patterns of litter decomposition, microbial and invertebrate biomass, and nutrient (especially nitrogen) availability. Nonnative terrestrial plant species are one of the most significant mediators of these global changes. This is likely to be particularly true in headwater streams, which are heavily influenced by the surrounding riparian vegetation due to the relatively high inputs of allochthonous organic matter and the close interactions between aquatic and terrestrial environments (Anderson and Sedell, 1979; Webster and Benfield, 1986; Tank et al, 2010). In headwater areas often only 50% of the total coarse particulate organic matter (CPOM) that enters the stream is transported to higher order rivers (Anderson and Sedell, 1979). The retained CPOM in the headwater region is processed by microbes, macroinvertebrate shredders, and other organisms (Boling et al., 1975; LeRoy and Marks, 2006), releasing energy and nutrients critical to local ecosystem dynamics.

In the midwestern United States, riparian ecosystems are rapidly being colonized by nonnative species (Moerke and Lamberti, 2004; Poland and McCullough, 2006). Common buckthorn Rhamnus cathartica is a nonnative facultative wetland species introduced to the United States from Europe (Knight et al., 2007). It has spread over a large percentage of the northern Midwest United States, as well as parts of Colorado and southern Canada (Knight et al., 2007) and now accounts for up to 45% of the mean basal area of some forests (Mascaro and Schnitzer, 2007). Buckthorn alters soil chemistry (Heneghan et al., 2004) and has been hypothesized to facilitate earthworm invasions, negatively impact native terrestrial plants, and alter the community composition of birds and mammals (Knight et al., 2007). The leaves of common buckthorn decompose five to seven times faster than common native species (green ash Fraxinuspennsylvanica, and American elm Ulmus ammcana; Freund et al., 2013) in headwater streams. This rapid decomposition of common buckthorn is in contrast to many previously studied riparian invasive trees (e.g, eucalyptus (Eucalyptus globus), Canhoto and Graca, 1996; melaleuca (Melaleuca quinquenervia), Martin et al, 2010; Russian olive (Elaeagnus angustifolia), Mineau et al., 2012) that have very tough or waxy leaves that make them more recalcitrant to decomposition.

Once in the stream, both native and nonnative leaves are available to shredders that, in conjunction with microbes, convert the allocthonous energy and nutrients into forms more readily available to other organisms (Boling et al., 1975; Anderson and Sedell, 1979). In many spring-fed streams of the midwestern United States, Gammarus amphipods are among the most important and numerically dominant shredder species (Heard et al., 1999; Ruetz et al., 2002). Globally, there are at least 1870 species of freshwater amphipods (Vainola et al., 2008) and those in the genus Gammarus often account for a large percentage of the macroinvertebrate biomass in streams and rivers (MacNeil et al., 1997). Gammarus pseudolimnaeus is a common shredder in headwater streams throughout the midwestern United States (Heard et al., 1999; Ruetz et al., 2002; J. Freund, unpubl. data). As such the species provides a logical focus for an investigation into detrital processing of riparian leaf litter.

The feeding habits of shredders such as amphipods are dependent upon the quantity, timing, and quality of organic debris input into the stream (Anderson and Sedell, 1979; FeRoy and Marks, 2006). The quantity of the detritus is determined by the abundance and proximity of input sources. The timing of nutrient input is determined by the rates at which riparian trees lose their leaves as well as the rate at which those leaves decay. The decay rate is, in turn, influenced by the conditioning a leaf receives from fungi and bacteria within the stream (Suberkropp et al., 1983) as well as by shading from overhanging vegetation (Albarino et al., 2008). Bacteria and fungi digest compounds such as cellulose and lignin, thereby making more nutrients in the leaves available to macroinvertebrates (Anderson and Sedell, 1979; Nelson, 2011). Microbes have been shown to increase the decomposition rate of leaves by 3.5 to 4 times compared to leaves lacking such colonization (Riblett et al., 2005). Invertebrate shredders rely on the nutrients released by microbial decomposition and the microbial biofilm itself as food sources (Nelson, 2011). There is evidence that Gammarus amphipods both prefer and have higher survival and growth rates when fed microbially conditioned leaves of a variety of native tree species compared to unconditioned or sterilized leaves (Barlocher and Kendrick, 1973; Pockl, 1995). Finally, the quality of the leaves as a food source is influenced by the availability of nutrients such as nitrogen and phosphorus within the leaves (Irons et al., 1988; Tank et al., 2010), the abundance of tannins that can impact digestive efficiency (Ostrofsky, 1997; LeRoy et al., 2007), and the concentrations of lignin and lignocellulose (Webster and Benfield, 1986; Ostrofsky, 1997; Tank et al., 2010). Some shredders, including Gammams amphipods, have enzymes that facilitate digestion of lignin and lignocellulose (potentially acquired by consuming fungi, Barlocher and Porter, 1986) whereas other shredders (e.g., cranefly larvae in the genus Tipula) have a more alkaline midgut that may minimize the impact of tannins and other compounds that inhibit invertebrate feeding (Martin et al, 1980; Barlocher and Porter, 1986).

This study is part of a larger investigation into how a terrestrial nonnative species (common buckthorn) affects the input and flow of energy within an aquatic system. The objectives of this study were to determine: (1) whether amphipods (G. pseudolimnaeus) differed in their consumption of leaves of nonnative common buckthorn and native green ash before leaves were conditioned in the stream, (2) whether the consumption of each leaf species changed over time as the leaves were conditioned within the stream, and (3) how the relative consumption of conditioned leaves varied between the native and nonnative plant species.


The study was conducted at Carroll University's Greene Field Station (43[degrees]0'59"N, 88[degrees]18'47"W), Waukesha County, WI, in the fall of 2013 (Experiment 1) and 2015 (Experiment 2). In our study area, common buckthorn comprises 54% and green ash comprises 39% of the tree species along the stream reach, whereas buckthorn provides 24% and ash provides 69% of the total leaf biomass entering the stream (Freund et al., 2013). Amphipods {Gammarus pseudolimnaeus) are the most abundant shredder in the stream, comprising over 50% of the macroinvertebrates collected in leaf packs in Genesee Creek (J. Freund, unpubl. data).

To compare the preferences of amphipods for native or nonnative leaves, two separate experiments were conducted. Experiment 1 assessed the consumption of fresh, newly fallen leaves, and Experiment 2 measured the consumption of stream conditioned leaves. For both experiments naturally abscised leaves were collected in leaf fall nets placed near Genesee Creek throughout the fall. Nets were checked regularly throughout the experiment and collected leaves were pooled and mixed prior to processing. For Experiment 1, unconditioned leaves were used immediately after collection. For Experiment 2, collected leaves were dried at 50 C, then stored at 0 C until use. Leaf packs for stream conditioning were constructed by placing 15 g (ash) or 20 g (buckthorn) of leaves in a nylon-mesh bag (7 mm mesh diameter). A greater mass of buckthorn leaves was used to increase the likelihood of having usable leaves following the longest conditioning intervals. Bags were fully submerged and secured in Genesee Creek (approx, depth 20 cm) to be stream-conditioned, with methods paralleling those of Freund et al (2013) so that decomposition rates would be comparable. Leaf packs of both species were placed in the stream every 2 d for a period of 20 d, including day 0 leaf packs that were placed in the stream for 20 min on the day all leaf packs were collected (i.e., 0, 2, 4, ... 20 d, for 11 conditioning dates, total). In both experiments a hole-punch (diam: 28 [mm.sup.2]) was used to generate uniformly-sized leaf disks from unconditioned (Experiment 1) or conditioned (Experiment 2) leaves for feeding trials.

Amphipods were collected from Genesee Creek using kick nets 0-1 d prior to experimental trials to minimize any changes in diet or behavior resulting from captivity. In the laboratory amphipods were housed in stream water in a glass-fronted refrigerator at 11 C under ambient light. During feeding trials, a single amphipod of adult size (>8 mm) was placed in a petri dish (9 cm diameter, Experiment 1) or a weigh boat (3 cm diameter, Experiment 2) with one disk of either ash or buckthorn. We conducted 60 replicate trials for each leaf species in Experiment 1, and 20 replicate trials for each leaf species in each of the 11 conditioning days in Experiment 2. Buckthorn leaves were too decomposed to be used after 20 d of stream conditioning; therefore, this set was excluded from the experimental design. Ten control containers with leaves but no amphipods were also established for each treatment group to assess any potential loss of leaf material due to leaching or decomposition or to differences in leaf selection or cutting style in both experiments. The same technician cut the control and experimental disks for each day of conditioning within each species. Because unconditioned leaves tended to float, leaf disks in Experiment 1 were pinned to the bottom of the petri dish. Feeding trials were run overnight at 11 C. Consumption was measured approximately 21 h after the onset of each trial. Due to the smaller containers used in Experiment 2 to conserve refrigerator space, some amphipods were able to climb out of their respective containers and, more rarely, enter other containers, presumably by transferring from the rim of one container to the tray or to the rim of a neighboring container. Those containers with zero or two amphipods at the end of the experiment were removed from all subsequent analyses. There was no significant difference between species or between days of conditioning in the number of amphipods that escaped ([N.sub.ash] = 53, [N.sub.buckthorn] = 53) or joined ([N.sub.ash] = 11, [N.sub.buckthorn] = 4) containers (chi-square test, P > 0.05).

Upon the conclusion of trials, the leaf disks were photographed. A grid with 1 [mm.sup.2] markings was included in each image to scale measurements. The area of each leaf disk was measured using Image J software (National Institutes of Health). Based on results from a pilot study conducted concurrently with Experiment 1, two additional measurements were recorded in Experiment 2. First, the length of each amphipod (base of the antennae to base of the telson) was estimated using Image J to ensure that differences in leaf consumption were not correlated with amphipod size (i.e., that larger amphipods would eat more of the disk). There was no correlation between the length of the amphipod at the conclusion of the study and either the area or the mass of the conditioned leaf disks that was consumed in 21 h (Pearson's product moment correlations; area: [r.sup.2.sub.asb] = 0.014, [r.sup.2.sub.bucktllorn] = 0.028; mass: [r.sup.2.sub.ash] = 0.001, [r.sup.2.sub.buckthorn] = 0.083). Second, after the leaf disks were photographed, each disk was dried at 50 C for 48 h and the dry mass was measured with an analytical balance to allow two measures of consumption (mass and area).


Because there were significant differences in both the area and mass of the control disks between days of conditioning (ANOVA: buckthorn (area) [F.sub.9,88] = 4.93, P < 0.001; (mass) [F.sub.9,88] = 7.10, P < 0.001; ash (area) [F.sub.10,98] = 3.97, P < 0.001; (mass) [F.sub.10,98] = 19.34, P < 0.001), the proportion of the median control area (or mass) of leaf consumed was calculated as: 1-[(area or mass of each experimental disk)/(median area or mass of all control disks for that length of stream conditioning and species)]. In situations in which the remaining experimental leaf disk mass or area was larger than the median control disk (i.e., apparent proportion consumed <0, N = 9 cases), the proportion consumed was set to zero. All proportions were arcsine transformed prior to the statistical analyses described below (Sokal and Rohlf, 1995).

For Experiment 1, the proportion of the median unconditioned control leaf area consumed was compared between the two species using Welch's t-test, which does not assume equal population variances (Welch, 1938). For Experiment 2, a generalized linear model was constructed to compare the effect of tree species, days of conditioning, and the interaction between these two factors on the proportion of the median control leaf area or leaf mass consumed. Model effects were tested using a likelihood ratio chi-square analysis. Because the interaction terms were significant (see below), post-hoc pairwise comparisons based on the interaction between the factors were generated using least significant difference multiple comparisons. Within species, these comparisons were used to identify the homogeneous subset of days of conditioning with the highest proportion of mass or area consumed (hereafter 'days of highest consumption'; i.e., the days of conditioning with consumption levels that were not significantly different from one another, but where at least one day within the group was significantly different from the next highest value). Between species, the pairwise comparisons were used to compare the proportion of the median control area or mass consumed within each day of conditioning. All analyses were conducted in SPSS (version 22.0). Alpha values of 0.05 were considered statistically significant in all main analyses. A Bonferroni corrected alpha of 0.0005 was used to identify homogenous subgroups of days of conditioning (110 comparisons) and a Bonferroni corrected alpha of 0.005 was used to identify significant differences between ash and buckthorn at each day of conditioning (10 comparisons). Untransformed values (means [+ or -] 1 SE) are presented in graphs and text for ease of interpretation.


In Experiment 1 the proportion of the median control area of unconditioned buckthorn leaves consumed ([bar.x] = 0.07 [+ or -] 0.01) was not significantly different from that of unconditioned ash leaves ([bar.x] = 0.04 [+ or -] 0.01; t = 1.74, d.f. = 103.7, P = 0.085; Fig. 1A). The proportion of unconditioned leaf disk consumed for each species was very low (range: 0-0.18 (ash); 0-0.42 (buckthorn), with no measurable consumption in 25% of trials (15 of 60) with ash disks and 22% of trials (13 of 60) with buckthorn disks.

In Experiment 2 there was a significant interaction between the effects of leaf species and days of conditioning on the mean proportion of the median control area of conditioned leaves that was consumed (hereafter 'mean proportion of area consumed'; GLM, likelihood ratio [X.sup.2] = 39.248, d.f. = 9, P < 0.001; Fig. IB). Post-hoc comparisons indicated the days of highest consumption included 8 d for ash: days 6, 8, 10, 12, 14, 16, 18 and 20; and 3 d for buckthorn: days 8, 10, and 12. Pairwise comparisons between species indicated a significantly higher proportion of the area of conditioned buckthorn disks was consumed compared to ash disks following 0, 8 and 12 d of conditioning. There were no days in which amphipods consumed a significantly higher proportion of the area of conditioned ash disks compared to buckthorn disks (Table 1, Fig. 1B).

There was also a significant interaction between the effects of leaf species and days of conditioning on the mean proportion of the median control mass of conditioned leaves that was consumed (hereafter 'mean proportion of mass consumed'; GLM, likelihood ratio [X.sup.2] = 45.977, d.f. = 9, P < 0.001; Fig. 2). Post-hoc comparisons indicated the days of highest consumption for ash included 8 d: days 2, 4, 6, 8,10, 12,14, and 20. For buckthorn the range included 4 d: days 6, 8, 10, and 12. Pairwise comparisons between species indicated that amphipods consumed a significantly higher proportion of the median control mass of conditioned buckthorn disks compared to ash disks following 6, 10, and 12 d of conditioning. There were no days in which amphipods consumed a significantly higher proportion of the mass of conditioned ash disks compared to buckthorn disks (Table 1, Fig. 2).


Unconditioned leaves of both ash and buckthorn were rarely consumed (Fig. 1A), consistent with other findings that reflect the importance of bacterial and fungal conditioning to the feeding preferences of shredders (Friberg and Jacobsen, 1994; Graga et al, 2001; Grata and Cressa, 2010). When leaves were dried and then conditioned in the stream for varying periods of time, consumption of common buckthorn generally increased, peaked, and then decreased, as measured by the relative loss of both area and mass (Figs. 1B, 2). In contrast consumption of green ash generally increased and then remained more or less stable throughout the range of conditioning times (Figs. 1B, 2). While in the stream leaves likely experience: leaching of soluble compounds (Webster and Benfield, 1986), photodegradation (Kohler et al., 2002), priming with labile organic matter from phytoplankton or macrophytes (potentially mediated Guenet et al, 2010; Danger et al., 2013), microbial conditioning (Tank et al, 2007), physical fractionation (Webster and Benfield, 1986), and some macroinvertebrate consumption (Webster and Benfield, 1986). Many of these processes, as well as direct consumption by the experimental amphipods, are likely to be impacted by differences in the nutritional and structural properties of the leaves (Webster and Benfield, 1986; Tank et al, 2007; Grafa and Cressa, 2010).

Common buckthorn leaves are very thin and lack a waxy cuticle, factors hypothesized to contribute to their significantly faster decomposition compared to native green ash leaves in Genesee Creek (Freund et al., 2013). Recently abscised buckthorn leaves have a relatively low C:N ratio (e.g., 19.6 - 20.6 for leaf litter collected in WI; Miller, 2010), largely due to high concentrations of nitrogen in the leaves (Knight et al., 2007; Heneghan et al., 2002, 2006). Buckthorn leaves also contain the secondary metabolite emodin (Seltzner and Eddy, 2003). Under some circumstances, secondary metabolites have been found to stimulate microbial activity (Hattenschwiler and Vitousek, 2000). However, they may also inhibit some microorganisms (Chapin et al, 2011); Therefore, it is uncertain whether emodin influences the decomposition rate of buckthorn leaves. The simple act of drying and rewetting the leaves substantially changed their palatability, as evidenced by the difference in consumption by amphipods in Experiment 1 and day 0 conditioning in Experiment 2 (Fig. 1A, B). The decline in consumption of buckthorn in our study after approximately 12 d of conditioning (Figs. 1B, 2) may be an artifact of their rapid decomposition. Buckthorn leaves in leaf packs conditioned for 16 or 18 d were mostly decomposed and those conditioned for 20 d were entirely unusable. Therefore, as the length of conditioning progressed, leaves that were least decomposed within the leaf pack became disproportionately represented in trials because they were the only ones to retain enough structural integrity to generate leaf disks. These leaves may have been more recalcitrant to decomposition than other leaves in the pack or simply more protected from biotic and abiotic factors in the stream due to their position in the leaf pack. In a field setting it is likely that buckthorn leaves would not be retained in the stream for more than 2 w unless they were trapped in the center of dense debris dams or were otherwise unusually resistant to decomposition.

In contrast to buckthorn leaves, the leaves of green ash are thicker, have a moderately waxy cuticle, and are characterized by a strong vein structure and greater overall structural integrity. While direct comparisons are unavailable, litter from green ash collected in Colorado had a C:N ratio of 36.1 and a lignin litter fraction of 9.5% (Gray et al., 2010). Similarly, litter of the related white ash (Fraxinus americana) collected in Kentucky had a C:N ratio of 58.0 and lignin fraction of 10.7% (Arthur et al., 2012), values that are substantially higher than those reported for buckthorn in Wisconsin (C:N = 19.6 - 20.6; lignin = 3.5-3.8%; Miller, 2010). These comparisons should be interpreted with caution given the influence of the timing and method of leaf collection and chemical analysis as well as regional and seasonal differences in leaf chemistry. In Experiment 2, once ash leaves were conditioned for at least a few days, consumption by amphipods appeared to depend more on the part of the leaf available in the disk (i.e., low versus high proportion of large veins; Fig. 3) than it did on days of conditioning. Future studies would benefit from standardization of the amount of venation in the leaves. Microbial decomposition and physical fractionation was much less evident for ash leaves in leaf packs, and most leaves were still largely intact after as much as 20 d of conditioning. In a more formal investigation of in-stream decomposition in Genesee Creek, leaf packs of green ash retained over 50% of their initial biomass over 84 d, whereas buckthorn leaf packs had lost over 50% of their biomass after only 21 d (Freund et al., 2013).

Variation in the decomposition rate of leaves between these two species may have introduced an unintended variable because buckthorn leaves that were selected from the leaf packs to generate disks became less random as leaves decayed over longer conditioning times. We attempted to control for this variation by having the same person cut control and experimental disks for each day of conditioning for each species. By then comparing the area or mass consumed as a proportion of the median area or mass of the disks in the control group, we minimized intra-day variation in the level of decomposition and any experimenter bias for particular leaf types. However, some level of variability in the measured consumption between days of conditioning may have resulted from this approach. As noted above this is particularly likely to be true for buckthorn leaf packs stream-conditioned for 16 or 18 d.

With faster decomposition rates (Freund et al, 2013) and greater consumption by shredders, nutrients contained within buckthorn leaves are processed faster than ash leaves, changing the amount and timing of energy and nutrient input into the stream ecosystem. This is similar to patterns demonstrated with some other invasive riparian species (e.g., Moline and Poff, 2008; Arthur et al., 2012). The pattern we observed for buckthorn contrasts with the relatively steady flow of energy from green ash throughout the leaf fall period. Differences in how amphipods process the two leaf species are also likely to result in differences in the nature of converted organic material. With more complete consumption of buckthorn leaves (Fig. 3), the organic material in the leaf is generally converted to fine particulate organic matter (<1 mm) or dissolved organic matter, whereas the less complete consumption of green ash leaves should result in a higher proportion of coarse particulate organic matter (> 1 mm) being retained in the stream. The design of this experiment did not allow for assessment of amphipods' preferences for ash or buckthorn leaves, as each animal was presented with the leaves of only one species. However, the relative area or mass consumed at each level of stream conditioning should correlate with the amphipods' propensity to consume each species, as a function of both preference for and ability to eat the leaf disk. For leaves that had not been conditioned, the proportion of area consumed did not differ significantly between the two species (Fig. 1A). Following conditioning buckthorn was generally more completely consumed than ash (Fig. 3), with particularly substantial differences on conditioning days with the highest levels of consumption (i.e., days 6, 8, 10, 12; Table 1; Figs. 1B and 2). It is notable that only one ash disk out of 154 was completely consumed across all days of conditioning compared to 27 of 141 for buckthorn. Direct choice experiments will help to elucidate whether amphipods have actual preferences for leaves of buckthorn over ash.

Common buckthorn first appeared at the Greene Field Station between 1950 and 1963 and had fully colonized the riparian zone at our study site by the early 1970's (Freund et al., 2013). It currently comprises more than 50% of the trees over 10 cm diameter at breast height in the most heavily buckthorn-invaded reaches of the stream (Freund et al., 2013). As with most riparian forests throughout the upper Midwest, encroachment of common buckthorn will likely continue to increase over time because buckthorn alters its environment and decreases the ability of native trees to survive (Heneghan et al., 2004; Knight et al., 2007; Mascaro and Schnitzer, 2007). Simultaneously, the nonnative emerald ash borer Agrilus planipennis (EAB), is likely to impact both local and regional riparian ecosystems by increasing the mortality of green ash and other ash species, potentially by as much as 99% (Herms and McCullough, 2014). Since first being reported in Waukesha County, WI, in 2012, EAB has spread to at least 12 municipalities including the town of Genesee (WI EAB Data Source, 2016), and EAB-induced tree mortality is apparent in this study location in 2016 (S. Lewis, pers. observ.). Specific changes in tree communities due to EAB-induced ash mortality are currently difficult to predict (Kashian and Witter, 2011). In the short term ash mortality is expected to create gaps that allow more light to reach buckthorn seedlings and saplings and further encourage their growth (Gandhi and Herms, 2010). In aquatic ecosystems an influx of buckthorn leaves and concurrent decrease in native ash leaves is likely to result from these changes.

The more rapid decomposition and faster, more complete processing of buckthorn suggest the changes to riparian plant communities mediated by buckthorn and emerald ash borer in the upper Midwest will have significant impacts on aquatic ecosystems throughout the region. Our research suggests this is likely to include changes in the conversion of allochthonous organic matter to finer scale components and alterations to the timing of energy and nutrient availability. The specific nature of these impacts will require a greater understanding of several factors, including the dynamics of leaf deposition and retention within the stream (Moline and Poff, 2008; Tank et al., 2010), and the impact of native and nonnative plant species on the energetics, reproduction, and survival of microbial decomposers, amphipods, and other shredder species.

Acknowledgments.--The authors thank M. Baumann, A. Ellickson, M. Lockhart, M. McCarthy, T. Neils, I. Perez, D. Rekah Suma, S. Suhr, and K. Williams for assistance with specimen collection, leaf processing and data collection. Funding for the project was provided by Carroll University, including donations from J. and S. Harrits that support research at the Greene Field Station. The manuscript was greatly improved by feedback from anonymous reviewers.


Albarino, R., V. D. Villanueva, and C. Canhoto. 2008. The effect of sunlight on leaf litter quality reduces growth of the shredder Klapopteryx kuscheli. Freshwater Biol., 53:1881-1889.

Anderson, N. H. and J. R. Sedell. 1979. Detritus processing by macroinvertebrates in stream ecosystems. Annu. Rev. Ecol. Syst., 24:351-377.

Arthur, M. A., S. R. Bray, C. R. Kuchle, and R. W. McEwan. 2012. The influence of the invasive shrub, Lonicera maackii, on leaf decomposition and microbial community dynamics. Plant Ecol,., 213:1571-1582.

Barlocher, F. and B. Kendrick. 1973. Fungi and food preferences of Gammarus pseudolimnaeus. Arch. Hydrobiol., 72:501-516.

--and C. W. Porter. 1986. Digestive enzymes and feeding strategies of three stream invertebrates. J. N. Am. Benthol. Soc., 5:58-66.

Benner, R. and Opsahl, S. 2001. Molecular indicators of the sources and transformations of dissolved organic matter in the Mississippi river plume. Org. Geochem., 32:597-607.

Boling Jr., R. H., E. D. Goodman, J. A. Van Sickle, J. O. Zimmer, K. W. Cummings, R. C. Petersen, and S. R. Reice. 1975. Toward a model of detritus processing in a woodland stream. Ecology, 56:141-151.

Canhoto, C. and M. A. S. Graca. 1996. Decomposition of Eucalyptus globulus leaves and three native leaf species (Alnus glutinosa, Castanea sativa and Quercus faginea) in a Portuguese low order stream. Hydrobiologia, 333:79-85.

Chapin F. S., Ill, P. A. Matson, and P. Vitousek. 2011. Principles of terrestrial ecosystem ecology. Springer- Verlag, New York. 529 p.

Danger, M., J. Cornut, E. Chauvet, P. Chavez, A. Elger, and A. Lecerf. 2013. Benthic algae stimulate leaf litter decomposition in detritus-based headwater streams: a case of aquatic priming effect? Ecology, 94:1604-1613.

Freund, J. G., E. Thobaben, N. Barkowski, and C. Reijo. 2013. Rapid in-stream decomposition of leaves of common buckthorn (Rhamnus cathartica), an invasive tree species. J. Freshwater Ecol., 28:355-363.

Friberg, N. and D. Jacobsen. 1994. Feeding plasticity of two detritivore-shredders. Freshwater Biol., 32:133-142.

Gandhi, K. J. K. and D. A. Herms. 2010. Direct and indirect effects of alien insect herbivores on ecological processes and interactions in forests of eastern North America. Biol. Invasions, 12:389-405.

Graca, M. A. S., and C. Cressa. 2010. Leaf quality of some tropical and temperate tree species as food resource for stream shredders. Int. Rev. Hydrobiol., 95:27-41.

--, --, M. O. Gessner, M. J. Feio, K. A. Callies, and C. Barrios. 2001. Food quality, feeding preferences, survival and growth of shredders from temperate and tropical streams. Freshwater Biol., 46:947-957.

Gray, C. M., R. K. Monson, and N. Fierer. 2010. Emissions of volatile organic compounds during the decomposition of plant litter. J. Geophys. Res., 115:G03015. doi:10.1029/2010JG001291.

Guenet, B., M. Danger, L. Abbadie, and G. Lacroix. 2010. Priming effect: bridging the gap between terrestrial and aquatic ecology. Ecology, 91:2850-2861.

Hattenschwiler, S. and P. M. Vitousek. 2000. The role of polyphenols in terrestrial ecosystem nutrient cycling. Trends Ecol. Evol, 15:238-243.

Heard, S. B., G. A. Schultz, C. B. Ogden, and T. C. Griesel. 1999. Mechanical abrasion and organic matter processing in an Iowa stream. Hydrobiologia, 400:179-186.

Heneghan, L., C. Clay, and C. Brundage. 2002. Rapid decomposition of buckthorn litter may change soil nutrient levels. Ecol. Rest., 20:108-111.

--, F. Fatemi, L. Umek, K. Grady, K. Fagen, and M. Workman. 2006. The invasive shrub European buckthorn (Rhamnus cathartica, L.) alters soil properties in Midwestern US woodlands. Appl. Soil Ecol, 32:142-148.

--, C. Rauschenberg, F. Fetemi, and M. Workman. 2004. European buckthorn (Rhamnus cathartica) and its effects on some ecosystem properties in an urban woodland. Ecol. Rest., 22:275-280.

Herms, D. A. and D. G. McCullough. 2014. Emerald ash borer invasion of North America: history, biology, ecology, impacts, and management. Annu. Rev. Entomol 59:13-30.

Irons, J. G. Ill, M. W. Oswood, and J. P. Bryant. 1988. Consumption of leaf detritus by a stream shredder: influence of tree species and nutrient status. Hydrobiologia, 160:53-61.

Kashian, D. M. andJ. A. Witter. 2011. Assessing the potential for ash canopy tree replacement via current regeneration following emerald ash borer-caused mortality on southeastern Michigan landscapes. Forest Ecol. Manag., 26:480-488.

Knight, K. S., J. S. Kurylo, A. G. Endress, J. R. Stewart, and P. B. Reich. 2007. Ecology and ecosystem impacts of common buckthorn (Rhamnus cathartica): a review. Biol. Invasions, 9:925-937.

Kohler, S., I. Buffam, A. Jonsson, and K. Bishop. 2002. Photochemical and microbial processing of stream and soil water dissolved organic matter in a boreal forested catchment in northern Sweden. Aquat. Sci., 64:269-281.

Kominoski, J. S., J. J. Follstad Shah, C. Canhoto, D. G. Fischer, D. P. Giling, E. Gonzalez, N. A. Griffiths, A. Larranaga, C. J. LeRoy, M. M. Mineau, Y. R. McElarney, S. M. Shirley, C. M. Swan, and S. D. Tiegs. 2013. Forecasting functional implications of global changes in riparian plant communities. Front. Ecol. Environ., 11:423-432.

LeRoy, C. J. and J. C. Marks. 2006. Litter quality, stream characteristics and litter diversity influence decomposition rates and macroinvertebrates. Freshwater Biol, 51:605-617.

--, T. G. Whitham, S. C. Wooley, andJ. C. Marks. 2007. Within-species variation in foliar chemistry influences leaflitter decomposition in a Utah river. J. N. Am. Benthol. Soc., 26:426-438.

MacNeil, C., J. T. A. Dick, and R. W. Elwood. 1997. The trophic ecology of Gammarus spp. (Crustacea Amphipoda): problems and perspectives concerning the functional feeding group concept. Biol. Rev., 72:349-364.

Martin, M. M., J. S. Martin, J. J. Kukor, and R. W. Merritt. 1980. The digestion of protein and carbohydrate by the stream detritivore, Tipula abdominalis (Diptera, Tipulidae). Oecologica, 46:360-364.

Martin, M. R., P. W. Tipping, and K. R. Reddy. 2010. Comparing native and exotic litter decomposition and nutrient dynamics. J. Aquat. Plant Manag., 48:72-79.

Mascaro, J. and S. A. Schnitzer. 2007. Rhamnus cathartica L. (common buckthorn) as an ecosystem dominant in southern Wisconsin forests. Northeast. Nat., 14:387-402.

Miller, S. N. 2010. Effects of Rhamnus cathartica (common buckthorn) stand age on decomposition. Undergraduate thesis, Carthage College. Kenosha, WI. < handle/123456789/157/Samantha%20Miller.pdf?sequence=1>. Accessed 31 May 2016.

Mineau, M. M., C V. Baxter, A. M. Marcarelli, and G. W. Minshall. 2012. An invasive riparian tree reduces stream ecosystem efficiency via a recalcitrant organic matter subsidy. Ecology, 93:1501-1508.

Moerke, A. H. and G. A. Lamberti. 2004. Restoring stream ecosystems: lessons from a midwestern state. Restar. Ecol., 12:327-334.

Moline, A. B. and N. L. Poff. 2008. Growth of an invertebrate shredder on native (Populus) and non-native (Tamarix, Elaeagnus) leaf litter. Freshwater Biol, 53:1012-1020.

Nelson, D. 2011. Gammarus-microbial interactions: a review. Int. J. Zool. doi:10.1155/2011/295026.

Ostrofsky, M. L. 1997. Relationship between chemical characteristics of autumn-shed leaves and aquatic processing rates. J. N. Am. Benthol. Soc., 16:750-759.

Pockl, M. 1995. Laboratory studies on growth, feeding, moulting and mortality in the freshwater amphipods Gammarus fossa-rum and G. roeseli. Arch. Hydrobiol., 134:223-253.

Poland, T. M. and D. G. McCullough. 2006. Emerald ash borer: invasion of the urban forest and the threat to North America's ash resource. J. Forest., 104:118-124.

Riblett, S. G., M. Palmer, and D. W. Coats. 2005. The importance of bacterivorous protists in the decomposition of stream leaf litter. Freshwater Biol., 50:516-526.

Ruetz, C. R., R. M. Newman, and B. Vondracek. 2002. Top-down control in a detritus-based food web: fish, shredders, and leaf breakdown. Oecologia, 132:307-315.

Seltzner, S. and T. L. Eddy. 2003. Allelopathy in Rhamnus cathartica, European buckthorn. Mich. Botanist, 42:51-61.

Sokal, R. R. and F. J. Rohlf. 1995. Biometry: the principles and practice of statistics in biological research, 4th ed. W. H. Freeman and Co., New York. 937 p.

Suberkropp, K., T. L. Arsuffi, andJ. P. Anderson. 1983. Comparison of degradative ability, enzymatic activity, and palatability of aquatic hyphomycetes grown on leaf litter. Appl. Environ. Microbiol., 46:237-244.

Tank, J. L., E. J. Rosi-Marshall, N. A. Griffiths, S. A. Entrekin, and M. L. Stephen. 2010. A review of allochthonous organic matter dynamics and metabolism in streams. J. North Am. Benthological Soc., 29:118-146.

Vainola, R., J. D. S. Witt, M. Grabowski, J. H. Bradbury, K. Jazdzewski, and B. Sket. 2008. Global diversity of amphipods (Amphipoda; Crustacea) in freshwater. Hydrobiologia, 595:241-255.

Webster, J. R. and E. F. Benfield. 1986. Vascular plant breakdown in freshwater ecosystems. Annu. Rev. Ecol. Syst., 17:567-594.

Welch, B. L. 1938. The significance of the difference between two means when the population variances are unequal. Biometrika, 34:29-35.

Wisconsin's Emerald Ash Borer Data Source. Confirmed EAB finds in Wisconsin by county and municipality. C>. Accessed 2016 February 16.




Department of Life Sciences, Carroll University, Waukesha, Wisconsin 53186

(1) Corresponding author: e-mail:

(2) Present address: Texas A&M University-Galveston, 200 Seawolf Parkway, Galveston, Texas 77554

Caption: Fig. 1.--(A) There was no significant difference between the mean proportion of area consumed for unconditioned green ash and common buckthorn disks (t-test, P = 0.085). (B) For conditioned leaves, the mean proportion of area consumed was significantly impacted by the interaction between leaf species and days of conditioning (GLM, likelihood ratio [X.sup.2] = 39.248, df = 9, P < 0.001). * Indicates significant differences between the two species for a specific day of conditioning. Bars below the x-axis indicate the days of highest consumption for each species. See text for more details

Caption: Fig. 2.--For conditioned leaves of common buckthorn and green ash, the mean proportion of mass consumed differed significantly depending on the number of days the leaves had been conditioned (GLM, likelihood ratio [X.sup.2] = 45.98, df=9, P < 0.001). * Indicates significant differences between the two species for a specific day of conditioning. Bars below the x-axis indicate the days of highest consumption for each species. See text for more details

Caption: Fig. 3.--A representative image of (A) green ash and (B) buckthorn, illustrating differences in the patterns of disc consumption after 14 (ash) or 8 (buckthorn) days of conditioning and 21 h of Gammarus feeding
TABLE 1.--Pairwise post-hoc comparisons of the arcsine transformed
proportion of the median control area and mass of native green ash
and nonnative common buckthorn consumed for each day of stream
conditioning. Negative mean differences indicate comparisons in
which consumption of ash > buckthorn


Days of stream     Mean difference
conditioning         [+ or -] SE           P

0                 0.59 [+ or -] 0.12    <0.001 *
2                -0.01 [+ or -] 0.13     0.933
4                -0.01 [+ or -] 0.13     0.945
6                 0.32 [+ or -] 0.13     0.017
8                 0.41 [+ or -] 0.13     0.001 *
10                0.34 [+ or -] 0.13     0.008
12                0.60 [+ or -] 0.12    <0.001 *
14               -0.07 [+ or -] 0.121    0.530
16                0.06 [+ or -] 0.13     0.657
18               -0.02 [+ or -] 0.12     0.880


Days of stream     Mean difference
conditioning         [+ or -] SE          P

0                 0.31 [+ or -] 0.12    0.013
2                -0.28 [+ or -] 0.13    0.038
4                -0.27 [+ or -] 0.14    0.063
6                 0.58 [+ or -] 0.14   <0.001 *
8                 0.24 [+ or -] 0.13    0.069
10                0.59 [+ or -] 0.14   <0.001 *
12                0.37 [+ or -] 0.13    0.005 *
14               -0.14 [+ or -] 0.12    0.262
16                0.04 [+ or -] 0.14    0.757
18                0.27 [+ or -] 0.13    0.038

* Significant at Bonferroni corrected [alpha] = 0.005.
COPYRIGHT 2017 University of Notre Dame, Department of Biological Sciences
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 2017 Gale, Cengage Learning. All rights reserved.

Article Details
Printer friendly Cite/link Email Feedback
Author:Lewis, Susan E.; Freund, Jason G.; Beaver, Morgan
Publication:The American Midland Naturalist
Article Type:Report
Geographic Code:1USA
Date:Jan 1, 2017
Previous Article:The phenology and spatial distribution of cavity-nesting hymenoptera and their parasitoids in a California Oak-Chaparral landscape mosaic.
Next Article:Community-level impacts of management and disturbance in Western Michigan Oak Savannas.

Terms of use | Privacy policy | Copyright © 2018 Farlex, Inc. | Feedback | For webmasters