Urban Archipelago Limits Goldenrod Gall Fly Distribution
Khalil Malcolm1 and Robert Warren II1*
1SUNY Buffalo State University, 1300 Elmwood Avenue, Buffalo, NY 14222 USA. *Corresponding author.
Urban Naturalist, No. 61 (2023)
Abstract
Land use and climate shift along urban-rural gradients – generally with temperature and habitat fragmentation increasing with increased urbanization. Many large cities arose adjacent to large water bodies, however, and the water bodies themselves create coastal-to-interior thermal gradients—generally with terrestrial temperature increasing nearer the water. These overlapping gradients, in turn, influence suitable habitat for temperature-dependent plants and animals. Eurosta solidaginis (Goldenrod Gall Fly) is a small gall fly with a larval stage occurring entirely inside the tissue of a single plant genus, Solidago (Goldenrod; Asteraceae). During diapause at northern latitudes, E. solidaginis larvae are exposed to considerable temperature extremes, with higher survival and fecundity in colder temperatures. We surveyed Solidago patches of various sizes in Western New York (US) to determine how the distribution of E. solidaginis corresponded with an urban-to-rural gradient embedded within a coastal-to-interior gradient. The probability of finding E. solidaginis galls increased with proximity to rural areas and in larger patches, with the lowest occupation in small urban patches. Patch size did not matter in rural areas, however, suggesting less dispersal limitation. The presence of E. solidaginis also increased with distance to the city center and the lake, both of which are relatively warmer, suggesting that the warmer temperatures negatively impacted the gall fly presence. Overall, these results suggest that gall fly distribution across an urban archipelago of Solidago patches is consistent with the predictions of island biogeography theory: E. solidaginis presence decreased with distance from the rural landscape and in smaller urban patches.
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Urban Archipelago Limits Goldenrod Gall Fly Distribution
Khalil Malcolm1 and Robert Warren II1*
Abstract - Land use and climate shift along urban-rural gradients – generally with temperature and habitat fragmentation increasing with increased urbanization. Many large cities arose adjacent to large water bodies, however, and the water bodies themselves create coastal-to-interior thermal gradients—generally with terrestrial temperature increasing nearer the water. These overlapping gradients, in turn, influence suitable habitat for temperature-dependent plants and animals. Eurosta solidaginis (Goldenrod Gall Fly) is a small gall fly with a larval stage occurring entirely inside the tissue of a single plant genus, Solidago (Goldenrod; Asteraceae). During diapause at northern latitudes, E. solidaginis larvae are exposed to considerable temperature extremes, with higher survival and fecundity in colder temperatures. We surveyed Solidago patches of various sizes in Western New York (US) to determine how the distribution of E. solidaginis corresponded with an urban-to-rural gradient embedded within a coastal-to-interior gradient. The probability of finding E. solidaginis galls increased with proximity to rural areas and in larger patches, with the lowest occupation in small urban patches. Patch size did not matter in rural areas, however, suggesting less dispersal limitation. The presence of E. solidaginis also increased with distance to the city center and the lake, both of which are relatively warmer, suggesting that the warmer temperatures negatively impacted the gall fly presence. Overall, these results suggest that gall fly distribution across an urban archipelago of Solidago patches is consistent with the predictions of island biogeography theory: E. solidaginis presence decreased with distance from the rural landscape and in smaller urban patches.
Introduction
The urban-rural gradient can be a useful simplification of complex landscape patterning whereby the gradient follows a decline in land use intensity from a highly developed urban core toward residential suburbs and ending in less developed rural areas (McDonnell and Pickett 1990, McKinney 2008). Where human population is high, and hence human impacts on native ecosystems also are high, native species generally decline relative to less populated landscapes (Evans 2010, Lososová et al. 2012, Luck and Smallbone 2010). Human population density is often considered the underlying driver in the urban-rural gradient (Gaston 2010, Raciti et al. 2012, Wandl et al. 2014) based on the assumption that associated anthropogenic correlates (e.g., impervious surface, pollution, fragmentation) drive declines in species richness and abundance (Luck and Smallbone 2010, McDonnell and Hahs 2008, McDonnell and Pickett 1990, McKinney 2008). However, local and regional climate also changes along urban-rural gradients. Indeed, urban areas often create ‘heat islands’ that narrow the temperature range due to warmer nights and winters (Hamblin et al. 2017, Imhoff et al. 2010, Ward et al. 2016) resulting in urban temperatures that are 8–10°C greater than proximate rural areas (Angilletta Jr. et al. 2007, Imhoff et al. 2010).
In addition to the urban heat island effects, approximately half of the US population lives on the coasts of the Great Lakes, Atlantic Ocean or Pacific Ocean, and large water bodies create coastal-to-interior climate gradients (Osland et al. 2014, Wong et al. 2015, Tayyebi and Jenerette 2016). Terrestrial regions east of Laurentian Great Lakes water bodies (North America) are generally warmer and wetter than western regions at the same latitudes due to the thermal effects of the lakes (Eichenlaub 1979, Scott and Huff 1996, Vermette 2020). As a result, for example, these regions are climate refuges for plants that otherwise only grow at lower latitudes. Urban-rural and coastal-to-interior gradients are overlapping, and hence, not independent, however. For example, forest patch ant communities in Western New York (US) [east/southeast of Lakes Erie and Ontario] shifted with coastal-to-interior gradients; however, their maximum heat tolerance corresponded with the urban-to-rural gradient (Warren II et al. 2018). Urban development also creates landscape-level fragmentation of natural habitats (McKinney 2008, Mcdonald et al. 2008, Haddad et al. 2015). As a result, patches of suitable forest and field habitats within urban landscapes become isolated ‘islands’ within unsuitable urbanized habitat (Hobbs 1988, Olejniczak et al. 2018, Tee et al. 2018). Essentially, ecological patterns in urbanized landscapes may follow the theory of island biogeography (MacArthur and Wilson 1967) if the forest or field patches act as isolated island ‘archipelagos’ and rural natural areas as ‘mainland’ sources of colonizers. As a result, only the best dispersing plants and arthropods inhabit natural areas in core urban habitat, and relatively larger patches have relatively larger species richness in all habitats (Bolger et al. 2000, Tscharntke and Brandl 2004, Olejniczak et al. 2018).
For arthropods, urban warming can be a benefit or curse, depending on the species (Dale and Frank 2018 and references therein). For thermophilic arthropods, urban warming can make cities, particularly relatively colder-climate cities, more hospitable by simulating their warmer native climes (Robinet et al. 2012, Meineke et al. 2013, Youngsteadt et al. 2017). Conversely, for less- thermophilic species, urban warming can decrease habitat suitability (Youngsteadt et al. 2017, McGlynn et al. 2019, Piano et al. 2020). More importantly, for arthropods that depend on specific plant hosts, urban-induced changes in the presence, abundance, phenology and physiology of the urban host plants can disrupt interactions with the species that depend on them (Neil and Wu 2006, Tabea et al. 2016, Dale and Frank 2018). That is, for plant-dependent organisms, habitat suitability is largely based on the abundance of the host plant, making the climate influences on the host species the salient driver.
Herbivores require suitable host plants as much as suitable habitat (Becerra 2003, Zangerl and Berenbaum 2005, Thrall et al. 2012). Plants commonly evolve secondary chemical compounds and other defenses to deter insect attackers and insects, in return, co-evolve better attacks to overcome the defenses (Becerra 1997, Glendinning 2002, Karban and Agrawal 2002). Consequently, herbivores typically specialize on a limited number of plants with defenses that they can overcome (Erhlich and Raven 1965, Bernays and Graham 1988, Novotny et al. 2006). Gall-forming insects, and mites, generally parasitize plants by using chemical or physical attacks to initiate abnormal plant tissue growth (e.g., bulbous or spindle-shaped protrusions) on leaves, stems and other plant parts (Stone and Schönrogge 2003, Tooker et al. 2008, Harris and Pitzschke 2020). The plant tissue typically grows around the insect and mite eggs, which forms a protective layer that often also serves as food for hatched larvae. Most gall-forming species belong to wasp (Hymenoptera), midge (Diptera) and mite (Acarina) taxa, and their interaction with plants typically is very specialized and limited to specific taxa (Harris and Pitzschke 2020).
Eurosta solidaginis Fitch (Goldenrod Gall Fly; Diptera: Tephritidae) is a small fly that exclusively attacks and produces galls on a single plant geneus, Solidago (Goldenrod; Asteraceae), in the Northeastern and Midwestern US – almost exclusively with a single species, Solidago altissima L. [Tall Goldenrod/Late Goldenrod; Asterales: Asteraceae] (Uhler 1951, Abrahamson et al. 1989a, Abrahamson and Weis 1997). Adult E. solidaginis emerge from overwintering in Solidago galls in spring and mate on the Solidago plants. Whereas some researchers have found that E. solidaginis readily re-colonize Solidago patches where the flies had been eliminated (Abrahamson et al. 1989a, Cappuccino 1992), the flies appear to be quite dispersal limited, male and female adults only travelling approximately 6 m from the galls from which they emerged (Sumerford et al. 2000, Cronin et al. 2001). After verifying the appropriate host plant (Abrahamson et al. 1989a), the females subsequently oviposit fertilized eggs in the terminal buds of newly emerged Solidago ramets. Hatched larvae bore down into the meristem tissue and form a chamber, which begins forming a surrounding gall within weeks, and the larvae consume the plant tissue inside. By autumn, the gall grows into a large, spherical swelling in the Solidago stem within which the E. solidaginis larvae will overwinter in diapause. During diapause in the northern climates, E. solidaginis fly larvae are exposed to considerable seasonal and diurnal temperature extremes in the upright plant stem. In response, the larvae undergo dramatic physiological changes that mitigate or prevent freeze damage, allowing them to survive temperatures as low as -20 to -80°C (Irwin and Lee 2000, Yi and Lee 2003, Marshall and Sinclair 2018). The gall flies have higher survival and fecundity in colder temperatures, presumably because the larvae can maintain diapause and conserve energy that would otherwise go toward metabolic processes during warm periods (Abrahamson et al. 1989b, Irwin and Lee 2000).
The objective of this study was to investigate how the distribution of E. solidaginis corresponded with an urban-to-rural gradient embedded within a coastal-to-interior gradient. The project began with observations by the authors that E. solidaginis was absent (based on gall presence) from apparently suitable Solidago patches on an urban college campus and adjacent city park. We formed multiple competing hypotheses to explain the absence of E. solidaginis: (H1) given E. solidaginis fidelity to S. altissima (Uhler 1951, Abrahamson et al. 1989a, Abrahamson and Weis 1997), if urban environments select for non-host species of Solidago, then the gall fly would have fewer host plants; (H2) if E. solidaginis winter diapause is adversely effected by relatively warmer temperatures (Abrahamson et al. 1989b, Irwin and Lee 2000), then gall presence should decrease nearer the city center and the Great Lakes’ water bodies; (H3) given that E. solidaginis appears to be a poor disperser (Sumerford et al. 2000, Cronin et al. 2001), gall presence in the urban landscape should decrease with distance from rural areas and with greater patch fragmentation.
Methods
Study Site
The Western New York region (WNY) is bordered by Lake Erie (25,700 km2 area; 489 km3 volume) to the West and Lake Ontario (18,960 km2; 1,639 km3) to the North. Lakes Erie and Ontario are two of the largest freshwater lakes in the world (by area and volume), and they exert considerable effect on WNY temperature and precipitation (Eichenlaub 1979, Scott and Huff 1996, Vermette 2020). Most notably, the prevailing weather systems move west to east, and the lakes moderate temperatures, creating a gradient from warmer annual temperature in the coastal areas that dissipates moving inland (eastward). The Buffalo metropolitan area is located on the shore of Lake Erie, approximately 45 km south of Lake Ontario, and it is the primary urban center of WNY with a population of 257,000 and a city area of 136.0 km2. The metropolitan area creates a second temperature gradient with temperatures decreasing with distance from the city. Several studies have confirmed these climate gradients, and biological responses, at the scale used for this study (Olejniczak et al. 2018, Warren II et al. 2018, Vermette 2020, Warren and Vermette 2022).
Study Species
Eurosta solidaginis is a model organism for field biology and the study of insect physiology, ecology and evolution. Eurosta solidaginis is widespread in North America, from coast to coast, through the southern US to the middle latitudes of Canada (Abrahamson and Weis 1997). The Eurosta solidaginis has been heavily studied in regions near the study area used here, including southern Canada, central Pennsylvania and central New York (Uhler 1951, Abrahamson et al. 1989a, Cappuccino 1992). Eurosta solidaginis primarily feeds on Solidago altissima L. plants throughout its range, and exclusively feeds on S. altissima in the study region (Felt 1940, Uhler 1951, Abrahamson et al. 1989a). The Solidago genus includes approximately 77 widely distributed North American species that primarily occur in open habitats (e.g., old fields, roadsides, forest clearings) in the northern regions. Solidago altissima is a tall, yellow-flowered perennial that is common in the upper Midwestern and Northeastern US that spreads through rhizomes to form dense patches with dozens to hundreds of ramets. Several similar Solidago species, both taxonomically and morphologically, co-occur with S. altissima (“Canada Goldenrod complex”: S. gigantea, S. canadensis and S. rugosa – the major differentiating trait being the presence or arrangement of hairs and flowerhead bracts). We used The Plants of Pennsylvania for identification (Rhoads and Block 2007).
Sampling
We searched roadsides, parks and abandoned lots following approximately 70 km of urban and rural transects parallel and perpendicular with Lake Erie (Supplement A, available online at http://www.eaglehill.us/URNAonline2/suppl-files/urna-220-Warren-S1.pdf). As a general categorization, we considered ‘urban’ those areas < 10 km from the city center and ‘rural’ those areas > 10 km from the city center. We also designated patches as occurring at or near “forest edge,” “open field,” “roadside,” “urban edge” and “water’s edge.” We searched mid-September to early October, which is the blooming time for S. altissima in the region – making it easier to locate patches. Once located, we searched S. altissima patches for the presence of the spherical galls indicative of E. solidaginis (we collected a subset of galls to verify identification) and we identified the Solidago species. Solidago altissima is one of the later blooming goldenrods (aka the “Late Goldenrod”) and, of the 83 patches searched, we only found two patches with a Solidago species other than S. altissima (specifically, S. rugosa). We recorded GPS locations for each patch, and we visually categorized each patch size as small (1–60 m2); medium (61–500 m2) or large (501–10000 m2). We used the GPS locations to calculate each patch distance to the city center (Buffalo NY; 42.886421, -78.878132) and the nearest lakeshore. We also calculated the distance of each patch to its nearest neighbor.
Data Analysis
We evaluated gall presence as a function of the patch distance to the city center and the patch distance from the lake using a generalized linear models (GLM) assuming a binomial error distribution. Both distances could not be evaluated in the same model because they were collinear (VIF > 4.0; car package; Fox and Weisberg 2019). We fit the GLMs using an analysis of deviance (ANODEV) approach. ANODEV is a maximum likelihood approach whereby a GLM model is fit using an analysis of variance model with a chi-square test. Neither GLM model was overdispered (Φ <1.2). We included patch size (small, medium, large) as a covariable. We also included distance x patch size interaction terms. For post hoc comparisons of the ANODEV models, we used the “Tukey” option of the glht function in the multcomp package (Hothorn et al. 2008) using the R statistical program (R Development Core Team Version 3.5.1 2020).
Results
Most of the S. altissima patches with E. solidaginis present were located at the edges of forests in open fields or along roadsides (Fig. 1a). Fewer Solidago patches were occupied by E. solidaginis along urban edges (parking lots and other concrete land use) and along water. In urban areas, S. altissima patches were more scattered with the mean (±SE) distance between patches at 535±92 m whereas in rural areas the patches were 308±59 m apart (Fig. 1b).
A distance to city center x patch size interaction term indicated that the probability of a patch being occupied by the gall fly increased with distance to the city center faster in large patches than medium and increased more in medium than small (Table 1; Fig. 2). That is, large patches were more likely to be occupied by gall flies in more urban areas than medium patches, which were more likely to be occupied by gall flies in more urban areas than small patches.
Gall flies were more likely to occupy patches with greater distance from the lake (Table 2; Fig. 3). The lack of an interaction effect indicated that the likelihood of occupation did not depend on patch size. That said, the probability that a patch was occupied by gall flies was twice as high in large (80 ± 13%) than small (40 ± 7%) patches, with medium-sized patches intermediate between the two (Table 2; 65 ± 12%) [Fig. 4].
Discussion
Eurostus solidaginis (Goldenrod Gall Fly) presence decreased with urbanization, and that pattern appears driven by its poor dispersal abilities across a fragmented landscape and its intolerance of the relatively warmer winters associated with an urban heat island. We found its main host plant, Solidago altissima (Tall Goldenrod/Late Goldenrod) blooming throughout the urban and rural areas used in this study, suggesting that host species limitation did not explain E. solidaginis’s decrease in urban areas (H1). We also found that the probability of finding E. solidaginis in S. altissima patches declined with distance from both the city center and the lake, both of which are relatively warmer than rural and inland areas, suggesting that relatively warmer temperatures negatively impact winter diapause (H2/H3). Finally, E. solidaginis was more likely to be absent from smaller patches in urban areas but did not vary with patch size in rural areas, suggesting that the fly does not disperse well across the patchier urban fragments (relative to the rural areas where S. altissima is more widespread and patches nearer each other.)
Plants in the Canada Goldenrod complex, such as S. altissima produce 2000–13000 wind-dispersed seeds per ramet (Werner and Platt 1976, Matlack 1987)”plainCitation”:”(Werner and Platt 1976; Matlack 1987, making them vigorous colonizers of proximate habitats, particularly as non-native invaders in Europe (Abrahamson et al. 2005). Whereas we found S. altissima patches fewer and further apart in the urban relative to rural areas, wind- and bird-dispersed plants do not appear particularly limited across this urban landscape (Olejniczak et al. 2018). For E. solidaginis, the primary demarcation of suitable habitat is the presence of S. altissima. We found that E. solidaginis decreased in urban areas. If one conceptualizes the urban landscape as an ‘ocean’ of concrete and other inhospitable habitat, the S. altissima patches can be considered ‘islands’ of suitable habitat for E. solidaginis. As such, the first prediction from the theory of island biogeography is that, for poor dispersers, islands furthest from the ‘mainland’ (the rural landscape in this case) are the least likely to be colonized. Eurostus solidaginis is reported as quite dispersal limited (Sumerford et al. 2000, Cronin et al. 2001), fitting the results presented here. At about 10 km from the city center, the presence of E. solidaginis in S. altissima patches flips from absent in most patches to present in most patches (except in small patches where the transition is more gradual). These results suggest that those patches nearest rural areas may readily receive E. solidaginis colonizers whereas in the urban center, at a great distance from the rural ‘mainland,’ colonizers would have to come from multiple fly generations that have travelled hop-scotch through the urban matrix. Of course, that is assuming all patch sizes equal, which was not the case.
The second prediction of island biogeography theory is that smaller islands undergo higher extinction/extirpation rates than relatively larger islands. Of course, those extirpations can be ameliorated with closer proximity to the mainland where higher colonization rates offset local losses. We found a remarkably similar pattern in E. solidaginis presence. In large S. altissima patches, E. solidaginis only was limited with increased urbanization, and a similar pattern occurred in with medium-sized patches. In small patches, however, E. solidaginis presence very gradually increased moving closer to rural areas, suggesting high extirpation across the gradient and low colonization in the core urban areas. In Ontario, Canada, Start and Gilbert (2016) reported island biogeography patterning in interactions between a specialist wasp parasitoid and E. solidaginis with fewer wasp attacks in small, isolated S. altissima patches. Bode and Maciejewski (2014) and Bode and Gilbert (2016) also conceptualized the Buffalo urban area as an ‘archipelago’ of S. altissima patches surrounded by unsuitable habitat, and both reported higher herbivore diversity on larger ‘islands.’ Bode and Maciejewski (2014) noted, however, that because S. altissima spreads locally through rhizome growth, patch size and age might be confounded. However, in our surveying of urban S. altissima patches, we found them bounded by concrete and landscaping (e.g., mowing) so that further rhizomatous spread would be difficult, if not impossible.
Poor dispersal might not be the only trait limiting E. solidaginis in urban areas. During winter diapause, a period in which the larvae can freeze solid, the energetic cost of warming limits fly health and survival (Irwin and Lee 2000, Marshall and Sinclair 2018). Given that urban areas create heat islands (Angilletta Jr. et al. 2007, Imhoff et al. 2010) that can adversely impact arthropods (Youngsteadt et al. 2017, McGlynn et al. 2019, Piano et al. 2020), we expected a decline in E. solidaginis with proximity to the city center. Of course, that patterning could be confounded by patch isolation rather than thermal climate, as well as the overlapping coastal-to-interior gradient created by the city center’s proximity to a great lake. Large bodies of water ameliorate temperature extremes, and annual temperatures are warmer with closer proximity to the lake (Eichenlaub 1979, Scott and Huff 1996; Vermette 2020). For this reason, we specifically sampled haphazard transects parallel as well as perpendicular to the lake in both urban and rural areas. Our results showed that the probability of finding E. solidaginis in S. altissima patches increased with distance from both city center and lake shore; however, the lack of interaction between distance from lake shore and patch size suggested that patch isolation was not a factor in the rural landscape. Certainly, other gradients may be embedded in this pattern, including changes in parasitoids and predators proximate to the lake, but it is suggestive of a thermal gradient pattern. Moreover, the lake climate effects are not simply annual. Conditions nearest the lake are relatively colder than inland during spring and relatively warmer than inland during autumn (but relatively warmer annually overall) so that impacts on S. solidaginis may be specific to a certain life history stage (as they are with ants in the same region; Warren II et al. 2018).
We found the distribution of E. solidaginis in S. altissima patches in an urban landscape consistent with the predictions of island biogeography theory. The probably of finding E. solidaginis galls increased with proximity to rural areas and in larger patches. More telling was the interaction between these dynamics resulting in the lowest occupation in small patches at the city core. We incorporated a sampling pattern to account for the heat island effect, which would be expected to be highest at the city core, and our results suggested that urban warming might contribute toward this pattern. In the end, the paucity of E. solidaginis at the urban core was not limited by its host plant but instead by the size and isolation of the host plant patches. A coastal-to-interior thermal gradient embedded in the urban-rural gradient may have added warming as a detriment to the overwintering gall fly.
Acknowledgments
We thank Derek Beahm and the Buffalo State Department of Biology Honors Program for support of this project. We also thank two anonymous reviewers for helpful comments on the manuscript.
Data Accessibility
The data generated and analyzed for the current study are available in the SUNY Buffalo State Digital Commons [http://digitalcommons.buffalostate.edu].
Declaration
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Literature Cited
Abrahamson, W.G., K.B. Dobley, H.R. Houseknecht, C.A. Pecone. 2005. Ecological divergence among five co-occurring species of old-field goldenrods. Plant Ecol 177:43–56. https://doi.org/10.1007/s11258-005-2069-2.
Abrahamson, W.G., K.D. McCrea, S.S. Anderson. 1989a. Host Preference and Recognition by the Goldenrod Ball Gallmaker Eurosta solidaginis (Diptera: Tephritidae). The American Midland Naturalist 121:322–330. https://doi.org/10.2307/2426036.
Abrahamson, W.G., J.F.Sattler, K.D.McCrea, A.E. Weis. 1989b. Variation in selection pressures on the Goldenrod Gall Fly and the competitive interactions of its natural enemies. Oecologia 79:15–22. https://doi.org/10.1007/BF00378234.
Abrahamson, W.G., and A.E. Weis. 1997. Evolutionary Ecology across Three Trophic Levels: Goldenrods, Gallmakers, and Natural Enemies (MPB-29). Princeton University Press, Princeton, NJ, USA.
Angilletta Jr., M.J., R.S. Wilson, A.C. Niehaus, M.W. Sears, C.A. Navas, and P.L. Ribeiro. 2007. Urban physiology: City ants possess high heat tolerance. PLoS ONE:e258.
Becerra, J.X. 2003. Synchronous coadaptation in an ancient case of herbivory. Proceedings of the National Academy of Sciences, USA 100:12804–12807.
Becerra, J.X. 1997. Insects on plants: macroevolutionary chemical trends in host use. Science 276:253–256.
Bernays, E.M., and M. Graham. 1988. On the evolution of host specificity in phytophagous arthropods. Ecology 69:886–892.
Bode, R.F., and A.B. Gilbert. 2016. Seed Predators, not Herbivores, Exert Natural Selection on Solidago spp . in an Urban Archipelago. Environ Entomol 45:150–154. https://doi.org/10.1093/ee/nvv158.
Bode, R.F., and A. Maciejewski. 2014. Herbivore biodiversity varies with patch sze in an urban archipelago. ijis 6:. https://doi.org/10.1177/IJIS.S13896.
Bolger, D.T., A.V. Suarez, K.R. Crooks, S.A. Morrison, and T.J. Case . 2000. Arthropods in urban habitat fragments in southern California: area, age, and edge effects. Ecol Appl 10:1230–1248.
Cappuccino, N. 1992. The Nature of Population Stability in Eurosta Solidaginis, A Nonoutbreaking Herbivore of Goldenrod. Ecology 73:1792–1801. https://doi.org/10.2307/1940030.
Cronin, J.T., K. Hyland, W.G. Abrahamson. 2001. The pattern, rate, and range of within-patch movement of a stem-galling fly. Ecological Entomology 26:16–24. https://doi.org/10.1046/j.1365-2311.2001.00294.x.
Dale, A.G., and S.D. Frank. 2018. Urban plants and climate drive unique arthropod interactions with unpredictable consequences. Current Opinion in Insect Science 29:27–33. https://doi.org/10.1016/j.cois.2018.06.001.
Eichenlaub, V.L. 1979. Weather and Climate of the Great Lakes Region. University of Notre Dame Press, Notre Dame, IN . USA.
Erhlich, P.R., and P.H. Raven. 1965. Butterflies and plants: a study in coevolution. Evolution 19:586–608.
Evans K.L. 2010. Individual species and urbanisation. Pp 53–87, In K.J. Gaston K.J. (Ed.). Urban Ecology. Cambridge University Press, Cambridge, UK.
Felt, E.P. 1940. Plant Galls and Gall Makers. Comstock Publishing Company, Inc., Ithaca, NY . USA.
Fox, J., and S. Weisberg. 2019. A companion to Applied Regression. Sage Publications, Inc., Thousand Oaks, CA, USA. 577 pp.
Gaston KJ. 2010. Urbanization. Pp 10-34, In K.J. Gaston (Ed.). Urban Ecology. Cambridge University Press, Cambridge, UK,
Glendinning, J.I. 2002. How do herbivorous insects cope with noxious secondary plant compounds in their diet? Entomologia Experimentalis et Applicata 104:15–25
Haddad, N.M., Brudvig LA, Clobert J, Kendi F. Davies, Andrew Gonzalez, Robert D. Holt, Thomas E. Lovejoy, Joseph O. Sexton, M.P. Austin, C.D. Collins, W.M. Cook, E.I. Damschen, R.M. Ewers, B.L. Foster, C.N. Jenkins, A.J. King, W.F. Laurance, D.J. Levey, C.R. Margules, B.A. Melbourne, A.O. Nicholls, J.L. Orrock, D.-X. Song, and J.R. Townshend. 2015. Habitat fragmentation and its lasting impact on Earth’s ecosystems. Science Advances 1:e1500052. https://doi.org/10.1126/sciadv.1500052.
Hamblin, A.L., E. Youngsteadt, M.M. Lopez-Uribe, and S.D Frank. 2017. Physiological thermal limits predict differential responses of bees to urban heat-island effects. Biology Letters 13:20170125.
Harris, M.O., and A. Pitzschke. 2020. Plants make galls to accommodate foreigners: some are friends, most are foes. New Phytologist 225:1852–1872. https://doi.org/10.1111/nph.16340.
Hobbs, E.R. 1988. Species richness of urban forest patches and implications for urban landscape diversity. Landscape Ecol 1:141–152. https://doi.org/10.1007/BF00162740.
Hothorn, T., F. Bretz, and P. Westfall. 2008. Simultaneous inference in general parametric models. Biom J 50:346–363. https://doi.org/10.1002/bimj.200810425.
Imhoff, M.L., P. Zhang, R.E. Wolfe, and L. Bounoua. 2010. Remote sensing of the urban heat island effect across biomes in the continental USA. Remote Sensing of Environment 114:504–513.
Irwin, J.T., and R.E. Lee Jr. 2000. Mild winter temperatures reduce survival and potential fecundity of the Goldenrod Gall Fly, Eurosta solidaginis (Diptera: Tephritidae). J Insect Physiol 46:655–661. https://doi.org/10.1016/S0022-1910(99)00153-5
Karban, R., and A.A. Agrawal. 2002. Herbivore offense. Annual Review of Ecology and Systematics 33:641–664.
Lososová, Z., M. Chytry´, L. Tichy´, J. Danihelka, K. Fajmon, O. Hajek, K. Kintrova, D. Lanikova, Z. Oty´pkova, and V. Rˇehorˇek. 2012. Biotic homogenization of Central European urban floras depends on residence time of alien species and habitat types. Biological Conservation 145:179–184.
Luck, G.W., and L.T. Smallbone. 2010. Species diversity and urbanisation: Patterns, drivers, implications. Pp 88–119, In K. Gaston (Ed.). Urban Ecology. Cambridge Univesity Press, Cambridge, UK.
MacArthur, R.H., and E.O. Wilson. 1967. The Theory of Island Biogeography. Princeton University Press, Princeton, NJ, USA. 224 pp.
Marshall, K.E., and B.J. Sinclair. 2018. Repeated freezing induces a trade-off between cryoprotection and egg production in the Goldenrod Gall Fly, Eurosta solidaginis. Journal of Experimental Biology 221:eb.177956. https://doi.org/10.1242/jeb.177956.
Matlack, G.R. 1987. Diaspore Size, Shape, and Fall Behavior in Wind-Dispersed Plant Species. American Journal of Botany 74:1150–1160. https://doi.org/10.2307/2444151.
Mcdonald, R.I., P. Kareiva, and R.T.T Forman. 2008. The implications of current and future urbanization for global protected areas and biodiversity conservation. Biological Conservation 141:1695–1703. https://doi.org/10.1016/j.biocon.2008.04.025
McDonnell M.J., and S.T.A. Pickett. 1990. Ecosystem structure and function along urban-rural gradients: An unexploited opportunity for ecology. Ecology 71:1232-1237.
McDonnell, M.J., and A.K. Hahs. 2008. The use of gradient analysis studies in advancing our understanding of the ecology of urbanizing landscapes: current status and future directions. Landscape Ecology 23:1143–1155.
McGlynn, T.P., E.K Meineke., C.A.Bahlai, E.Li, E.A. Hartop, B.J. Adams and B.V. Brown. 2019. Temperature accounts for the biodiversity of a hyperdiverse group of insects in urban Los Angeles. Proceedings of the Royal Society B: Biological Sciences 286:20191818. https://doi.org/10.1098/rspb.2019.1818.
McKinney, M. 2008. Effects of urbanization on species richness: A review of plants and animals. Urban Ecosystems 11:161–176.
Meineke, E.K., R.R. Dunn, J.O. Sexton, and S.D. Frank. 2013. Urban Warming Drives Insect Pest Abundance on Street Trees. PLOS ONE 8:e59687. https://doi.org/10.1371/journal.pone.0059687.
Neil, K., and J. Wu. 2006. Effects of urbanization on plant flowering phenology: A review. Urban Ecosyst 9:243–257. https://doi.org/10.1007/s11252-006-9354-2
Novotny, V., P. Drozd, S.E. Miller, M. Kulfan, M. Janda, Y. Basset, and G.D. Weiblen. 2006. Why are there so many species of herbivorous insects in the tropical rainforests? Science 313:1115–1118.
Olejniczak, M., D.J. Spiering, D.L. Potts, and R.J. Warren II. 2018. Urban forests form isolated archipelagos. Journal of Urban Ecology 4:1–8
Osland, M.J., N. Enwright, and C.L. Stagg. 2014. Freshwater availability and coastal wetland foundation species: Ecological transitions along a rainfall gradient. Ecology, 95, 2789-2802.
Piano, E., F. Bona, and M. Isaia. 2020. Urbanization drivers differentially affect ground arthropod assemblages in the city of Turin (NW-Italy). Urban Ecosystem 23:617–629. https://doi.org/10.1007/s11252-020-00937-z.
R Development Core Team Version 3.5.1 . 2020. R: A Language and Environment for Statistical Computing.
Raciti, S.M., L.R. Hutyra, A.C. Finzi. 2012. Inconsistent definitions of 'urban' result in different conclusions about the size of urban carbon and nitrogen stocks. Ecological Applications 22:1015–1035.
Rhoads, A.F., and T.A. Block. 2007. The Plants of Pennsylvania, 2nd edn. University of Pennsylvania Press, Philadelphia, USA. 1042.
Robinet, C., C.-E. Imbert, J. Rousselet J, D. Sauvard, J. Garcia, F. Goussard, and A. Roques. 2012. Human-mediated long-distance jumps of the pine processionary moth in Europe. Biol Invasions 14:1557–1569. https://doi.org/10.1007/s10530-011-9979-9.
Scott, R.W., and F.A. Huff. 1996. Impacts of the Great Lakes on regional climate conditions. Journal of Great Lakes Research 22:845–863.
Start, D., and B. Gilbert. 2016. Host–parasitoid evolution in a metacommunity. Proceedings of the Royal Society B: Biological Sciences 283:20160477. https://doi.org/10.1098/rspb.2016.0477.
Stone, G.N., and K. Schönrogge. 2003. The adaptive significance of insect gall morphology. Trends in Ecology and Evolution 18:512–522. https://doi.org/10.1016/S0169-5347(03)00247-7.
Sumerford, D.V., W.G. Abrahamson, and A.E. Weis. 2000. The effects of drought on the Solidago altissima-Eurosta solidaginis-natural enemy complex: population dynamics, local extirpations, and measures of selection intensity on gall size. Oecologia 122:240–248. https://doi.org/10.1007/PL00008852.
Tabea, T., S. Dirk, and K. Eva. 2016. Effects of urbanization on direct and indirect interactions in a tri-trophic system. Ecol Appl 26:664–675. https://doi.org/10.1890/14-1787
Tayyebi, A., and G.D. Jenerette. 2016. Increases in the climate change adaption effectiveness and availability of vegetation across a coastal to desert climate gradient in metropolitan Los Angeles, CA, USA. Science of the Total Environment:548–549, 60–71.
Tee, S.L., L.D. Samantha, N. Kamarudin, Z. Akbar, A.M. Lechner, A. Ashton-Butt, and B. Azhar. 2018. Urban forest fragmentation impoverishes native mammalian biodiversity in the tropics. Ecol Evol 8:12506–12521. https://doi.org/10.1002/ece3.4632.
Thrall, P.H., A.L. Laine, M. Ravensdale, A.Nemri, P.N. Dodds, L.G. Barrett, and J.J. Burdon. 2012. Rapid genetic change underpins antagonistic coevolution in a natural host-pathogen metapopulation. Ecology Letters 15:425–435.
Tooker, J.F., J.R. Rohr, W.G. Abrahamson, and C.M.D. Moraes. 2008. Gall insects can avoid and alter indirect plant defenses. New Phytologist 178:657–671. https://doi.org/10.1111/j.1469-8137.2008.02392.x.
Tscharntke, T., R. Brandl. 2004. Plant-insect interactions in fragmented landscapes. Annual Review of Entomology 49:405–430.
Uhler, L.D. 1951. Biology and Ecology of the Goldenrod Gall Fly: Eurosta Solidaginis (Fitch). Cornell University Agricultural Experiment Station, Ithaca, NY, USA. 51 pp.
Vermette, S.J. 2020. Western New York’s (WNY’s). five climate zones. Proceedings of the Rochester Academy of Science 21:23–37.
Wandl, D.I.A., V. Nadin, W. Zonneveld, and R. Rooi. (2014) Beyond urban -rural classifications: Characterising and mapping territories-in-between across Europe. Landscape and Urban Planning 130:50-63.
Ward, K., S. Lauf, B. Kleinschmit, and W. Endlicher. 2016. Heat waves and urban heat islands in Europe: A review of relevant drivers. Science of the Total Environment:569–570, 527–539.
Warren II, R.J., S. Bayba, and K. Krupp. 2018. Interacting effects of urbanization and coastal gradients on ant thermal responses. Journal of Urban Ecology 4:1.
Warren, R.J., and S. Vermette. 2022. Laurentian Great Lakes warming threatens northern fruit belt refugia. Int J Biometeorol 66:669–677. https://doi.org/10.1007/s00484-021-02226-6
Werner, P.A., and W.J. Platt. 1976. Ecological Relationships of Co-Occurring Goldenrods (Solidago: Compositae). The American Naturalist 110:959–971.
Wong, G.J., E.C. Osterberg, R.L. Hawley, Z.R. Courville, D.G. Ferris, and J.A. Howley. 2015. Coast-to-interior gradient in recent northwest Greenland precipitation trends (1952 -2012). Environmental Research Letters 10:114008.
Yi, S.-X., R.E. Lee. 2003. Detecting freeze injury and seasonal cold-hardening of cells and tissues in the gall fly larvae, Eurosta solidaginis (Diptera: Tephritidae) using fluorescent vital dyes. Journal of Insect Physiology 49:999–1004. https://doi.org/10.1016/S0022-1910(03.00168-9.
Youngsteadt, E., A.F. Ernst, R.R. Dunn, and S.D. Frank. 2017. Responses of arthropod populations to warming depend on latitude: evidence from urban heat islands. Global Change Biology 23:1436–1447. https://doi.org/10.1111/gcb.13550.
Zangerl, A.R., and M. Berenbaum. 2005. Increase in toxicity of an invasive weed after reassociation with its coevolved herbivore. Proceedings of the National Academy of Sciences, USA 102:15529–15532.