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Spatial and Temporal Variability in Aquatic-Terrestrial Trophic Linkages in a Subtropical Estuary

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Spatial and Temporal Variability in Aquatic-Terrestrial Trophic Linkages in a Subtropical Estuary Spatial and temporal variability in aquatic-terrestrial trophic linkages in a subtropical estuary Thesis Presented in Partial Fulfillment of the Requirements for the Degree Master of Science in the Graduate School of The Ohio State University By Martha Jeannette Zapata, B.S. Graduate Program in Environment and Natural Resources The Ohio State University 2018 Thesis Committee: Dr. S. Mažeika P. Sullivan, Advisor Dr. Suzanne M. Gray Dr. Lauren M. Pintor Copyright by Martha Jeannette Zapata 2018 Abstract Estuaries and coastal wetlands are highly productive ecosystems that support unique biodiversity and complex food webs. The movement of organisms among habitats is a critical facilitator of biological connectivity in estuaries, however, little attention has been directed towards biological connectivity between aquatic and terrestrial zones. Although a substantial body of research has documented aquatic insect emergence as a critical nutritional subsidy between rivers and their adjacent riparian zones that is essential to the functioning of both ecosystems, our understanding of this food-web linkage in estuaries remains unresolved. My research aimed to characterize emergent (i.e., adult) aquatic insects and insect- facilitated subsidies to terrestrial consumers (i.e., orb-web spiders) across the Fakahatchee Strand and Ten Thousand Islands Estuary of southwestern Florida. Emergent aquatic insects and nearshore orb-weaving spiders were surveyed during the summer and winter seasons of 2015 and 2016 at nine study reaches (i.e., sites) representing upper, mid, and lower segments of the estuary, generally corresponding with freshwater, mesohaline, and polyhaline habitats, respectively. Salinity, as well as a suite of additional physicochemical parameters including dissolved oxygen, temperature, total dissolved solids, pH; nutrients (total nitrogen, nitrate, total phosphorus, phosphate); and shoreline habitat were also measured. These data were used to address the following questions: (1) How do the density, community composition, and individual traits of emergent aquatic insects vary seasonally across an estuarine salinity gradient, and how ii are these characteristics related to the distribution and condition of nearshore orb-weaving spiders? (2) How are trophic dynamics (aquatically-derived nutritional subsidies, trophic position) of riparian spiders associated with spatial and temporal variability in estuaries as mediated by emergent insect subsidies? Abnormally-high rainfall induced by El Niño-Southern Oscillation (ENSO) led to salinity levels that deviated from typical winter months. Emergent insect density varied by season and estuary position (linear mixed model [LMM]: F1,37 = 8.57, P = 0.006 and F2,5.8 = 8.75, P = 0.018, respectively), but was generally higher during the winter. Overall, emergence rates were highest at mid-estuary reaches during the winter (x̅ ± SE, 17.9 ± 5.8) and lowest at lower-estuary reaches during both the summer (x̅ ± SE, 1.89 ± 2.81) and winter (x̅ ± SE, 4.22 ± 1.98). Season was a strong predictor of Shannon diversity (LMM: F1,36 = 15.645, P < 0.001), Pielou’s evenness (LMM: F1,31.8 = 5.316, P = 0.028), and richness (families) of emergent insects (LMM: F1,36 = 26.353, P < 0.001) most notably at lower-estuary sites where measures were higher during the winter. Water temperature, and phosphate and total nitrogen concentrations also received support as predictors of emergence rate (R2 = 0.19, F = 5.77, P = 0.024). Community composition varied spatially across the estuarine gradient (ANOSIM: R = 0.158, P = 0.001), and showed a marginal seasonal difference only at lower-estuary habitats (ANOSIM: R= 0.1023, P = 0.061). Insect communities were largely dominated by Chironomidae, which accounted for 53-56% of variation in community composition across the estuarine gradient. Spatial and seasonal patterns in density of Dolichopodidae also contributed to the observed community differences. Mean body size of Chironomidae and Dolichopodidae were generally 180 and 400% larger, respectively, at lower-estuary habitats compared to upper-estuary counterparts. At lower-estuary iii reaches, emergent aquatic insects exhibited lower dispersal ability and higher prevalence of univoltinism than upper- and mid-estuary assemblages. Orb-weaving spider density tracked emergent insects, with densities at mid-estuary reaches exceeding those of the upper- and lower-estuary, There was also a seasonal effect on orb-web density (LMM: F1,84.8 = 16.692, P < 0.0001), particularly at mid-estuary reaches where densities were higher during the winter than the summer (P < 0.0001). Estuary position strongly influenced body condition of Tetragnatha, which was 96% higher in the lower-estuary than in the upper-estuary (LMM: F2,19.50 = 11.254, P = 0.0006). Leucage body condition was strongly influenced by a season x position interaction (LMM: F2,348.31 = 2.506, P = 0.083), whereby individuals exhibited higher body condition during the winter at upper- (P = 0.046) and mid- estuary (P < 0.0001) habitats. Bayesian mixing models using δ13C and δ15N signatures of primary producer sources and consumers showed that aquatically-derived energy (i.e., nutritional subsidies originating from epiphyton and phytoplankton) represented 0.79 to 0.99 of the diet of nearshore spiders across all study reaches and seasons. Reliance on aquatically-derived energy varied spatially (LMM: F1,174 = 358.57, P < 0.0001) and was higher overall at mid- and lower-estuary reaches than in the upper-estuary (Tukey HSD, P < 0.05). For the most common family of spiders, Tetragnathidae, reliance on aquatically-derived energy was slightly greater in winter (0.89) than summer (0.79) at FW and PH reaches (0.99 v. 0.94, respectively). Estuary position (LMM: F2,.6.31 = 57.420, P < 0.0001) and season (LMM: F1,172.94 = 128.947, P < 0.0001) also exerted strong effects on spider trophic position. Spiders occupied higher trophic positions during the summer at upper- and mid- estuary reaches (Tukey HSD, P < 0.0001), whereas trophic positions were consistently lower at iv lower-estuary reaches. δ13C of orb-weaving spiders trended with δ13C of Chironomidae during 2 the summer (R = 0.52, F1,4 = 6.401, P = 0.065), but not during the winter (P > 0.05), suggesting that Chironomidae is an important dietary component and vector of aquatically-derived energy at least during some time periods. Together, these findings contribute to our understanding of aquatic insect community structure and function in estuarine ecosystems. Wet-dry seasonal hydrology and ENSO events appear to drive emergent insect communities, largely via effects on salinity concentrations but also through effects on nutrients and water temperature. In addition, these results have important implications for subsidy dynamics in estuaries. In this study, spatial and temporal variability in the density and traits of emergent insects were related to nearshore spiders, and thus are likely to also mediate the distribution and trophic characteristics of a suite of other terrestrial insectivores including bats, birds, lizards and influence trophic-mediated ecosystem processes including nutrient cycling, biomagnification of contaminants, and maintenance of biodiversity. An improved understanding of seasonal subsidy dynamics in estuaries may help forecast and manage functional ecosystem responses to environmental disturbances (e.g., sea level rise). For example, artificial lighting at night (ALAN) is projected to increase in intensity alongside human population density in coastal areas. ALAN has been shown to affect emergent aquatic insect communities as well as riparian orb-weaving spiders. I conclude the thesis with a review of potential impacts that ALAN may pose in estuaries, from individual- to ecosystem-scale effects. v Acknowledgments I would like to extend my wholehearted thanks to Scott Glassmeyer, Jessica Espinoza, Reina Tyl, Edna Fernandez, S.J. Kwiatkowski, David O’Neill, and Ben Rubinoff for their assistance and support with field sampling and lab processing. Thank you all for your hard work and good spirit in the field. To Patrick O’Donnell of the Rookery Bay National Estuarine Research Reserve – thank you for collaborating with us on this research, sharing extensive knowledge of the Ten Thousand Islands region, and teaching me how to safely navigate through the maze of mangroves. Thanks to all the folks at Rookery Bay NERR and Fakahatchee Strand Preserve State Park, including Bob Sebold, Julie Drevenkar, Kevin Cunniff, Britta Johnson, Mike Owens, Karen Schanzle. for moral and logistical support. Thank you to Lars Meyer, Kristen Diesburg, and David Manning of STRIVE Lab for gracious assistance with logistical planning, insect identification, and statistical analysis. To my committee members Dr. Suzanne Gray and Dr. Lauren Pintor – your insights and expertise were helpful in the development of my project from beginning to end. To my family Ana, Rodrigo, and Rodannie Zapata— thank you for always encouraging me to follow my passions and supporting me whenever I was stuck in the mangroves without a paddle. Finally, I extend deep gratitude to my advisor Dr. Mažeika Sullivan. Thank you for your patient encouragement and guidance during the past 3.5 years of this collaboration. Thank you for believing in me as a student and offering me the opportunity to grow personally and as a scientist. vi Vita 2008…………………………… Barbara Goleman Senior High School 2013…………………………… B.S. Marine Biology, Florida International University 2014…………………………… Graduate
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