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Spatial variation in trophic ecology of small mammals in wetlands: support for hydrological drivers Jorista van der Merwe1,2,† and Eric C. Hellgren1,3 1Cooperative

Wildlife Research Laboratory, Southern Illinois University, Carbondale, Illinois 62901 USA of Biological Sciences, Arkansas Tech University, Russellville, Arkansas 72801 USA 3Department of Wildlife Ecology and Conservation, University of Florida, Gainesville, Florida 32611 USA 2Department

Citation: van der Merwe, J., and E. C. Hellgren. 2016. Spatial variation in trophic ecology of small mammals in wetlands: support for hydrological drivers. Ecosphere 7(11):e01567. 10.1002/ecs2.1567

Abstract. Food webs composed of similar consumers can vary based on nutrient input, habitat structure,

and other factors. For wetland-associated species, fluctuating water levels can potentially affect habitat quality, which in turn can affect trophic diversity. Our objective was to determine spatiotemporal variation in the trophic structure of small mammals at two wetland complexes (floodplain and mineland) in southern Illinois. We live-trapped small mammals during 2011–2013 at nine wetland patches on the Mississippi River floodplain and 14 patches at a reclaimed mineland. We collected hair samples from six species of small mammals (n = 428) at these wetland complexes. We analyzed C and N stable isotopes for three mammal taxa (Oryzomys palustris, Peromyscus spp., Microtus ochrogaster) to compare diet between species, sites, and times. Food sources (vegetation and invertebrates) were collected to form the isotopic baseline. We found no seasonal difference in diet composition, but isotopic values varied between sites and species. At the floodplain site, both δ15N and δ13C isotopic values for Oryzomys were more variable and completely enclosed that of Peromyscus. At the mining site, Peromyscus were at a lower trophic level (δ15N) and had a separate and less variable δ13C values from Oryzomys. Microtus was at a lower trophic position than the other two species at both sites. These results point to reduced niche overlap between Oryzomys and Peromyscus at the mining site, perhaps due to lower habitat quality and limited suitable resources. At the floodplain site, we conclude that more dynamic hydrology gave rise to higher biodiversity and more resources allowing small mammals to use similar food items. Key words: food webs; habitat; isotopes; Oryzomys; Peromyscus. Received 22 September 2016; accepted 26 September 2016. Corresponding Editor: Robert Parmenter. Copyright: © 2016 van der Merwe and Hellgren. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. † E-mail: [email protected]

Introduction

are often located on floodplains of major rivers (Cowardin et al. 1979) and are therefore highly dynamic systems inhabited by unique faunal and floral assemblages of high species diversity and richness (Benke 2001). These floodplain wetlands can change seasonally and annually (Gosselink and Maltby 1990), with ephemeral wetlands forming or expanding in flood years and drying up in drought years. Fluctuating hydrology causes temporal resource pulses (Holt 2008), which in turn affects population sizes and facilitates competitive coexistence. Dispersal

Food webs involving similar consumers can vary depending on the nutrient inputs, the nature of the habitat in which the consumers occur, and the number and types of consumers at various trophic levels. In wetland systems, resources often vary spatially and temporally, and depending on the water permanence and proximity to large rivers, this variation can result in varying community assemblages (Schneider and Frost 1996, Spencer et al. 1999). Palustrine wetlands v www.esajournals.org

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November 2016 v Volume 7(11) v Article e01567

van der MERWE AND HELLGREN

allows animals to exploit these locally abundant resources and allows them to persist in areas that might otherwise be less suitable. Hence, resource pulses can sustain or increase species diversity, especially when occurring at an intermediate rate (Connell 1978). The intermediate disturbance hypothesis indicates that high diversity is maintained when species composition is continually changing and when disturbances occur at an intermediate rate and intensity (Connell 1978). Initially, as the interval between disturbances (e.g., flooding) increases, species diversity will increase because more time is available for species to establish, and slower growing species could persist to maturity. However, if the interval becomes too long, competitive exclusion will eliminate some of the weaker species (Connell 1978). The flood- pulse concept introduced by Junk et al. (1989) suggests that floodplain wetlands are more productive and have greater species diversity than river channels or man-made impoundments, mainly because of the fluctuating hydrology and associated nutrient inputs resulting from the flood pulses of the river. Accordingly, floodplain wetlands should have higher biodiversity than those wetlands with less dynamic hydrology. In addition to affecting biodiversity, dynamic hydrology (i.e., hydroperiod) can also influence species abundances; for example, abundances of aquatic invertebrate can increase with a longer hydroperiod (because of increased time to complete life cycles; Brooks 2000). Thus, arthropod abundance might be higher at stable, man- made wetlands, potentially leading to top-down effects on vegetation and bottom-up changes to secondary and tertiary consumers. The size and direction of these potential effects will depend on the presence of predators and their efficacy in exploiting their prey (Power 1992). Phragmites australis (hereafter Phragmites), which is considered an alien species in parts of its range and can become invasive in disturbed areas, is often associated with man-made wetlands and has been linked to trophic shifts at invaded wetlands (Gratton and Denno 2006). Herbivorous consumers excluded Phragmites from their diets, which resulted in a food web dependent on detritus feeders and detrital resources. In addition, dominance of Phragmites could encourage omnivorous consumers (e.g., small mammals) to v www.esajournals.org

consume more invertebrates because of lack of vegetation diversity, and thus lead to higher trophic position for these consumers. Accordingly, differences in biodiversity between a floodplain wetland complex and a mining-related wetland complex (because of differences in hydroperiod) might result in highly different food webs at the two wetland types. Stable-isotope techniques can provide a measure of trophic position that integrates energy flow through all trophic pathways leading to an organism, with the potential to capture complex trophic interactions in communities (Kling et al. 1992). The δ15N values from tissue samples of animals can be used to estimate trophic position because δ15N values of a consumer show stepwise enrichment with increases in trophic level (DeNiro and Epstein 1981). Carbon isotope values (δ13C) change little with trophic position but vary dramatically among primary producers (DeNiro and Epstein 1978, Post 2002). In terrestrial systems, δ13C values can be used to distinguish between diets based on plants that use C3 and C4 photosynthetic pathways (Peterson and Fry 1987). We compared stable-isotope ratios within small-mammal assemblages and their food sources at two hydrologically distinct wetland complexes among seasons over 3 years, with the overall goal of determining spatiotemporal variation in trophic position among species in this assemblage. Under the flood-pulse hypothesis (Junk et al. 1989, also Junk and Wantzen 2006), we hypothesized that small mammals at mining- related wetlands (more stable hydrology) would have greater niche separation, because of a lower diversity of food sources than in floodplain wetlands. We also expected that small mammals at floodplain-associated wetlands would have wider isotopic breadth than those at mining wetlands. Lastly, we predicted that higher arthropod abundances at mining-related wetlands would lead to food web changes, and specifically higher trophic position in omnivorous small mammals.

Materials and Methods Study area

The study was conducted at two wetland complexes in southern Illinois. One complex

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Fig. 1. Location of the two wetland complexes, one on the floodplain of the Mississippi River, and one at a reclaimed mining site, at which hair samples were collected from trapped small mammals, in southern Illinois 2011–2013.

percent of the total area is made up of water impoundments or wetlands (Delahunt 2011). The floodplain site was located at the Middle Mississippi River Wetland Field Station (hereafter floodplain site), an area of approximately 560 ha, managed by Southern Illinois University (SIUC) and located on the eastern side of the Mississippi River floodplain, 4 km ESE of Cape Girardeau, Missouri (37°17′2.08″ N; 89°28′6.37″ W). This area consisted of various managed natural wetlands within Cape Bend State Fish and Wildlife Area and the Shawnee National Forest. Because the floodplain site is located on the

was on a reclaimed surface mine in Jackson County, whereas the second site was on the Mississippi River floodplain, in Alexander County (Fig. 1). The mining site was the Illinois Department of Natural Resources CONSOL Energy—Burning Star 5 Wildlife area, a 3200-ha site (37°52′32.95″ N; 89°12′30.47″ W). Mining occurred at this site mostly after 1978, at which time reclamation of at least part of the mined areas was required by federal law. The area included roughly 1200 ha of wetland habitats and 650 ha of unmined forested areas and is located in the Big Muddy River watershed. Six v www.esajournals.org

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Cerling et al. 2006). In wolves (Canis lupus), isotope values of guard hairs reflect seasonal differences in their diet (Darimont and Reimchen 2002). Hair can distinguish temporal changes in diet, but also can distinguish spatial differences among populations of similar species. In particular, animals occurring in the same habitat type but at different locations might experience different environmental pressures or micro- habitat conditions that could be reflected in their diets. The frequency of molts has, to our knowledge, not been recorded in Oryzomys. If similar to golden mice (Ochrotomys nuttali; Linzey and Linzey 1967) or deer mice (Peromyscus spp.; Miller et al. 2008) then there should be one post-juvenile molt at 30–65 days of age as well as one to two adult molts during spring and fall. Therefore, we assumed guard hair represented an assimilation time of approximately 2–4 months. Because there is considerable variation in δ13C and δ15N values among different ecosystems, reference food items (invertebrates and vegetation) that form the base of the food web are needed to accurately compare food webs among systems. We collected potential food items at each patch during spring and fall sampling periods. We used a 0.3 m × 0.5 m, 500-μm mesh dip net to sample aquatic invertebrates in wetlands by sweeping the net along the edges of shallow water parallel to trap transects, and collecting all invertebrates in the net. We also collected all invertebrates found in or around Sherman traps, and by looking under debris along the traplines (Myers 2010). Invertebrates included insects (mainly Hemiptera, Coleop tera, Lepidoptera, and Orthoptera) and snails (Gastropoda). Plant material was collected by walking parallel to traplines along the wetland edges and collecting samples from all plant species encountered. Vegetation samples included samples from forbs, sedges, grasses, and any available seeds and fruits from shrubs and trees. This work was carried out in accordance with stipulations set forth by the Southern Illinois University Carbondale Institutional Animal Care and Use Committee (IACUC; Protocol 10-009). All materials were stored in a freezer until preparation for isotopic analysis. Hair was soaked in an acetone bath for 2 h. All samples

Mississippi River floodplain, periodic inundation occurs because of rises in river stage and because the water table is close to the surface (Jackson 2006). The dynamic characteristic of the floodplain (shorter hydroperiod) is a major difference between floodplain site and the mining site. Dominant vegetation also differed distinctly. All of the wetland patches at the mining site had Phragmites spp. At 10 of 14 patches, Phragmites was the dominant vegetation type. Few patches had a high diversity of emergent wetland vegetation present. In contrast, none of the wetland patches at the floodplain had stands of Phragmites, but rather were dominated by herbaceous Polygonum spp., and various other grasses including Echinochloa spp. and Bromus spp.

Data collection

Trapping and handling.—Trapping for small mammals took place at 14 wetland patches at the mining site and nine patches at the floodplain site. We trapped small mammals in each patch using 30–100 Sherman live traps (8 cm × 9 cm × 23 cm; H.B. Sherman Traps, Tallahassee, Florida, USA) four nights/week (session) every 8 weeks, resulting in four trapping sessions/year (once in spring [March–April], twice in summer [May–August], and once in fall [October– November]), from 2011 to 2013. This work was carried out in accordance with stipulations set forth by the SIUC Institutional Animal Care and Use Committee (IACUC; Protocol 10-009). Sample collection and isotope analysis.—We sampled guard hair from the dorsal area (Darimont and Reimchen 2002) from all small mammals captured during spring (March–April) and fall (October–November), and from rice rats during all seasons, for every year. Different animal tissues have different isotope fractionation (Tieszen et al. 1983), which also need to be considered when deciding on which material to use for stable-isotope analysis. Animal tissues most often used in stable-isotope analyses include blood, muscle or organ tissue, bone, hair, and fecal samples. Turnover rates vary among tissues, and the choice of material depends on the time frame of diet that is investigated. Hair is often used in stable-isotope analysis to describe the diet of mammals over the scale of months (Schwertl et al. 2003, Sponheimer et al. 2003, v www.esajournals.org

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were rinsed for 10 min in deionized water, then dried for at least 48 h at 60°C, after which samples were crushed to a powder and sub-samples (~2.0 mg for vegetation; ~0.35–0.45 mg for hair and invertebrates) were placed into tin capsules for analysis. Isotopes of C and N were analyzed using an Isotope Ratio Mass Spectrometer (IRMS: Delta V Plus, Thermo Fisher Scientific, Waltham, Massachusetts, USA) at SIUC. Samples were combusted into N2 + CO2 using a Costech 4010 ECS elemental analyzer. Isotope values were expressed as a delta (δ) notation relative to Pee Dee marine fossil limestone (carbon) and atmospheric nitrogen standards, respectively, using the following equation:

Table 1. Linear regression results for models describing δ15N variation of hair samples from Oryzomys and Peromyscus, invertebrates, and vegetation at floodplain and mining-related wetland complexes in southern Illinois, 2011–2013.

δX = (Rsample ∕Rstandard ) − 1) × 1000

K

Δ AICc

wi

Material × Site Material × Year Material Material × Season Site × Season Site × Year Site Season NULL Year

11 16 6 12 7 7 3 4 2 4

0.00 71.14 94.74 100.89 251.98 306.10 317.14 365.45 413.15 413.83

1.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00

Notes: Models are sorted from lowest to highest Akaike i nformation criterion (AICc) value. K represents the number of parameters in the model, and wi represents the Akaike weighting factor on the model.

where X is 13C or 15N. Rsample represents the ratio of heavier to lighter isotopes in the sample and Rstandard the similar ratio in the standard (Darimont and Reimchen 2002). Typically, hair samples are enriched in 15N by 1.4–3.4‰ in mammals (DeNiro and Epstein 1981), whereas 13C is enriched by approximately 0–1‰ in small mammals, relative to diet (DeNiro and Epstein 1978). Hair of white-footed mice (Peromyscus leucopus) was enriched in 15N by 2.9‰–3.3‰ (Miller et al. 2008, DeMots et al. 2010) and 13C enriched by 1.1‰ compared to diet (DeMots et al. 2010). We used an average diet-to- hair discrimination factor of 3.0‰ N and 1‰ C for Peromyscus, Oryzomys, and Microtus for mixing models, as is common in these types of studies (Steenweg et al. 2011, Weiser and Powell 2011, Osterback et al. 2015). Data analysis.—We developed a set of generalized linear models, assuming normal distribution, to determine whether mean δ15N or δ13C values (in separate model sets for each isotope) were affected by season (spring, summer [only for Oryzomys], fall), year (2011, 2012, 2013), site (floodplain, mineland), and type of material (Oryzomys, Peromyscus, invertebrates [pooled], vegetation), in different combinations as additive or interactive models (Tables 1 and 2). For generalized linear models examining δ13C differences, we excluded plant material from analyses, because δ13C is known to differ between C3 and C4 plants. After the global model was run and shown to fit the data, we used Akaike’s v www.esajournals.org

Model

information criterion, corrected for small sample bias (AICc) to find the model that best described variation in δ15N or δ13C over the 3-year study (Anderson 2008). For each model, we also calculated the Akaike weights (wi), which provides the weight of evidence in favor of model i. The closer to 1 the wi, the greater the support for that model. We used among-individual variance in stable isotopic values as an index of trophic niche breadth (Bearhop et al. 2004). We assumed that Table 2. Linear regression results for competing models describing δ13C variation of hair samples from Oryzomys and Peromyscus, and invertebrates at floodplain and mining-related wetland complexes in southern Illinois, 2011–2013. Model

K

Δ AICc

wi

Material × Year Material × Season Material Material × Site Site × Year Year Site × Season NULL Site Season

13 9 5 9 7 4 5 2 3 3

0.00 7.71 16.40 21.45 97.86 103.21 109.57 110.24 111.99 112.00

0.98 0.02 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00

Notes: Models are sorted from lowest to highest Akaike i nformation criterion (AICc) value. K represents the number of parameters in the model, and wi represents the Akaike weighting factor on the model.

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populations of Oryzomys and Peromyscus represented a mix of generalist A and B individuals (Bearhop et al. 2004), where individuals of a type A generalist species consume a constant proportion of multiple prey types, and individuals of a type B generalist species consume widely differing proportions of each prey item. A narrow breadth of isotopic values among individuals in such a population could be due to specialization on one or a few prey items, or all individuals feeding on a wide variety of items, but in very similar proportions such that the integrated average has a narrow variance. Under the prediction that populations of generalist species consuming a wide range of prey species (i.e., individuals within the species specializing on a number of different prey items) will exhibit greater variation than species populations consuming a narrow range of prey items, we compared isotopic niche breadth of Oryzomys and Peromyscus within and between each study area, for both isotopes, using Levene’s test of homogeneity of variance (Flaherty and Ben-David 2010).

and 39 invertebrate samples from the floodplain site; and 110 plant and 57 invertebrate samples from the mining site. The model that best described variation among mean δ15N values included an interaction between site and the type of material (i.e., whether it was Oryzomys, Peromyscus, Microtus, vegetation, or invertebrates; Table 1). Mean δ15N for Oryzomys differed by only ~1‰ between the two sites (Table 3, Fig. 2). Average hair isotope values varied little among samples over the course of 3 years, including little variation among seasons. The δ15N values of Oryzomys and Peromyscus spp. were similar at the floodplain site (F1,202 = 2.01, P = 0.16; Fig. 2). However, δ15N values of Oryzomys were higher than Peromyscus at the mining site (F2,214 = 4.96, P