Ecological Limits to Local Species Richness in Dusky Salamanders (Genus Desmognathus Baird)

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Ecological Limits to Local Species Richness in Dusky Salamanders (Genus Desmognathus Baird) Canadian Journal of Zoology Ecological limits to local species richness in dusky salamanders (genus Desmognathus Baird) Journal: Canadian Journal of Zoology Manuscript ID cjz-2016-0071.R2 Manuscript Type: Article Date Submitted by the Author: 06-Oct-2016 Complete List of Authors: Camp, C.D.; Department of Biology Wooten, Jessica; Centre College, Biology Graham, Sean; Sul Ross State University, Biology, Geology, and Physical Sciences Draft Pauley, Thomas; Marshall University, Biological Sciences species richness, ecological limits, GIS-based niche modeling, Appalachian Keyword: Mountains, Desmognathus https://mc06.manuscriptcentral.com/cjz-pubs Page 1 of 39 Canadian Journal of Zoology 1 1 Ecological limits to local species richness in dusky salamanders (genus Desmognathus 2 Baird) 3 4 Carlos D. Camp a, Jessica A. Wooten b*, Sean P. Graham c, Thomas K. Pauley d 5 6 aDepartment of Biology, Piedmont College, PO Box 10, Demorest, Georgia, USA 7 E-mail: [email protected] 8 bDepartment of Biology, Centre College, 600 West Walnut Street, Danville, Kentucky, USA 9 E-mail: [email protected] 10 cDepartment of Biology, Geology, and Physical Sciences, Sul Ross State University, Box C-64, 11 Alpine, Texas, USA Draft 12 E-mail: [email protected] 13 dDepartment of Biological Sciences, Marshall University, 1 John Marshall Drive, Marshall 14 University, Huntington, West Virginia, USA 15 16 *Corresponding author. Tel.: (859) 238-5322 17 E-mail address: [email protected] 18 19 20 21 22 23 https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 2 of 39 2 24 Abstract: Species richness commonly varies with elevation, but in many montane regions, the 25 greatest number of species occurs at middle elevations. A recent regional analysis showed this 26 pattern in Appalachian salamanders of the genus Desmognathus Baird. The authors proposed 27 that the phylogenetic niche conservatism of these salamanders causes species to accumulate at 28 intermediate elevations, which are characterized by the ancestral climate for the genus. They 29 further suggested that physiological tolerances limit dispersal into higher or lower elevations. We 30 tested this hypothesis using geographic information systems (GIS)-based analysis of 235 local 31 Desmognathus communities. Consistent with the regional analysis, local species richness was 32 greatest at middle elevations. However, the number of species is not limited by physiological 33 tolerances but appears to be restricted ecologically by climate variables favoring aridity as well 34 as by biotic factors. Whether such ecologicalDraft limits on species richness at the local level 35 influences richness across regions or evolutionary clades remains to be tested. 36 37 38 39 Key words: species richness, ecological limits, GIS-based niche modeling, Appalachian 40 Mountains, Desmognathus 41 42 43 44 45 46 https://mc06.manuscriptcentral.com/cjz-pubs Page 3 of 39 Canadian Journal of Zoology 3 47 Introduction 48 49 Biogeographers have long wondered why biodiversity is not randomly scattered across 50 the planet but occurs in certain regular, repeatable patterns. However, in spite of two centuries of 51 scholastic scrutiny punctuated by intensified research activity over the last several decades, no 52 consensus explanation has emerged (Rahbek 1997, 2005). In fact, more than 100 hypotheses 53 have been proposed to explain species-richness patterns across the surface of the globe (Palmer 54 1994). While empirical research has whittled down this number to a handful of credible 55 hypotheses, debate continues (Rahbek and Graves 2001). For example, Rabosky (2009) recently 56 proposed ecological limits as an alternative to evolutionary diversification (speciation minus 57 extinction) rates in explaining species-richnessDraft patterns across regions and evolutionary clades. 58 In a spirited rebuttal, Wiens (2011) pointed out that ecology cannot affect richness without 59 influencing rates of speciation, extinction, or dispersal. He further criticized Rabosky’s (2009) 60 evidence for ecological limits. 61 A well-documented relationship is that between species richness and elevation. Among 62 the more enigmatic facets of this relationship is that the number of species often peaks at 63 intermediate elevations (e.g., Colwell and Lees 2000; McCain 2004; Cardelús et al. 2006; Li et 64 al. 2009). While this pattern has been recognized for decades (Rahbek 1995), the underlying 65 cause, or suite of causes, remains unresolved. Included in the explanations hypothesized for this 66 phenomenon are environmental conditions favoring either co-existence (Heaney 2001) or 67 speciation (Smith et al. 2007), evolutionary time (Smith et al. 2007), population dynamics 68 (Kessler 2000), geographic area (Sanders 2002), or simply the central accumulation of species- https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 4 of 39 4 69 range overlaps resulting from their random shuffling within a geographically defined space (mid- 70 domain effect, Colwell et al. 2004). 71 In a recent analysis, Kozak and Wiens (2010) demonstrated mid-elevational peaks of 72 evolutionary lineages in several genera (i.e., genera Plethodon Tschudi and Desmognathus 73 Baird) of Appalachian salamanders. They further showed that mid-level elevations have been 74 occupied longer than either higher or lower elevations. They hypothesized that phylogenetic 75 niche conservatism in these salamanders (Kozak and Wiens 2006) restricts these lineages to their 76 ancestral climatic niches, which are currently associated with intermediate elevations. As 77 speciation occurs within this climatic zone, dispersal to higher and lower elevations is 78 physiologically constrained, resulting in an accumulation of a greater number of species at mid- 79 level elevations. Draft 80 Perceived patterns of species richness, however, vary with scale (Rahbek 2005), and 81 while local diversity ‒ i.e., species sympatric within the same community ‒ tends to reflect the 82 larger regional species pool (Harrison and Cornell 2008), it is at the local level where ecological 83 factors should affect species richness (Wiens 2011). Machac et al. (2011) showed that local 84 diversity may be constrained ecologically by both biotic and abiotic factors. Because the analysis 85 of Kozak and Wiens (2010) of salamanders was conducted at a regional scale across the 86 Appalachian Mountains, our purpose was to test their hypothesis at the level of the local 87 community. 88 We tested the hypothesis that species are physiologically restricted to the climates of 89 mid-elevations by using Geographic Information Systems (GIS)-based niche modeling. Driven 90 by recent advancements in computing power and the widespread availability of large, 91 environmental datasets, niche modeling has brought about a significant leap in understanding https://mc06.manuscriptcentral.com/cjz-pubs Page 5 of 39 Canadian Journal of Zoology 5 92 how climate and other factors regulate the geographical distribution of individual species (e.g., 93 Graham et al. 2004; Kozak et al. 2008). This technique, however, has infrequently been used to 94 address questions regarding spatial patterns of community structure (Stephens and Wiens 2009). 95 We chose the salamander genus Desmognathus , a speciose lineage of Appalachian 96 salamanders whose communities are strongly influenced by interspecific interactions (Bruce 97 2009, 2011). Specifically we use GIS-based niche modeling to answer the following questions. 98 1) Does species richness within local desmognathan communities peak at intermediate 99 elevations? 2) How does elevation relate to specific climatic variables? 3) What is the 100 relationship between local species richness and climatic variables? 4) Is the relationship between 101 species richness and climate constrained by physiological limits, i.e., is richness of local 102 communities defined entirely by the physiologicalDraft tolerances of individual component species? 103 104 Materials and methods 105 106 Study species 107 The dusky salamanders of the genus Desmognathus currently comprise 21 recognized, 108 named species (Table 1; http://amphibiaweb.org) of lungless salamander (family Plethodontidae Table 1 109 Gray), although additional unnamed, cryptic lineages exist (Beamer and Lamb 2008; Tilley et al. 110 2013; Tilley 2016). In a phylogenetic analysis of mtDNA sequences, Kozak et al. (2005) 111 identified 35 putatively independent, evolutionary lineages. This genus is distributed across most 112 of the eastern United States but is most speciose in the southern Appalachian Mountains where 113 up to six species can occur in together in a local community (Bruce 1991). Dusky salamanders 114 are typically associated with streams but vary widely in their microhabitat choice along moisture https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 6 of 39 6 115 gradients. In multi-species assemblages, with very few exceptions, each point along the gradient 116 is occupied by a species (or evolutionary lineage) possessing a unique ecomorph. Species range 117 from being large (adult body lengths = 90+ mm) and completely aquatic with multi-year larval 118 periods to completely terrestrial, miniature species (adult body lengths < 40 mm) having no 119 aquatic larval phase (Petranka 1998). All species prey on invertebrates with both larvae (e.g., 120 Burton 1976; Davic 1991; Beachy 1995) and adults (e.g., Martof and Scott 1957; Donovan and 121 Folkerts 1972; Fitzpatrick
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